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Forests are frequently exposed to natural disturbances, which are likely to increase with global change, and may jeopardize the delivery of ecosystem services. Mixed-species forests have often been shown to be more productive than monocultures, but it is unclear whether this results from mixed stands being in part more resistant to various biotic and abiotic disturbance factors. This review investigates the relationships between tree diversity and stand resistance to natural disturbances and explores the ecological mechanisms behind the observed relationships. Download full article here: http://www.springer.com/home?SGWID=0-0-1003-0-0&aqId=3315777&download=1&checkval=3718a7a79c09f728241d31ff367d3f0e
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FOREST ENTOMOLOGY (E BROCKERHOFF, SECTION EDITOR)
Tree Diversity Drives Forest Stand Resistance
to Natural Disturbances
Hervé Jactel
1
&Jürgen Bauhus
2
&Johanna Boberg
3
&Damien Bonal
4
&
Bastien Castagneyrol
1
&Barry Gardiner
5
&Jose Ramon Gonzalez-Olabarria
6
&
Julia Koricheva
7
&Nicolas Meurisse
8
&Eckehard G. Brockerhoff
9
#Springer International Publishing AG 2017
Abstract
Purpose of review Forests are frequently exposed to natural
disturbances, which are likely to increase with global change,
and may jeopardize the delivery of ecosystem services.
Mixed-species forests have often been shown to be more pro-
ductive than monocultures, but it is unclear whether this re-
sults from mixed stands being in part more resistant to various
biotic and abiotic disturbance factors. Thisreview investigates
the relationships between tree diversity and stand resistance to
natural disturbances and explores the ecological mechanisms
behind the observed relationships.
Recent findings Mixed forests appear to be more resistant
than monocultures to small mammalian herbivores, soil-
borne fungal diseases and specialized insect herbivores.
Admixing broadleaves to conifers also increases the resistance
to fire and windstorms when compared to pure conifer stands.
However, mixed forests may be more affected by drought
depending on the species in the mixture.
Summary Overall, our findings suggest that mixed forests are
more resistant to natural disturbances that are relatively small-
scale and selective in their effect. However, benefits provided
by mixtures are less evident for larger-scale disturbances.
This article is part of the Topical Collection on Forest Entomology
*Hervé Jactel
herve.jactel@inra.fr
Jürgen Bauhus
juergen.bauhus@waldbau.uni-freiburg.de
Johanna Boberg
johanna.boberg@slu.se
Damien Bonal
Damien.bonal@inra.fr
Bastien Castagneyrol
bastien.castagneyrol@inra.fr
Barry Gardiner
barry.gardiner@efi.int
Jose Ramon Gonzalez-Olabarria
jr.gonzalez@ctfc.es
Julia Koricheva
julia.koricheva@rhul.ac.uk
Nicolas Meurisse
nicolas.meurisse@scionresearch.com
Eckehard G. Brockerhoff
eckehard.brockerhoff@scionresearch.com
1
BIOGECO, INRA, University of Bordeaux, 33610 Cestas, France
2
Faculty of Environment and Natural Resources, University of
Freiburg, Tennenbacherstr. 4, 79106 Freiburg, Germany
3
Department of Forest Mycology and Plant Pathology, Swedish
University of Agricultural Sciences, PO Box 7026, 750
07 Uppsala, Sweden
4
Université de Lorraine, INRA, UMR EEF,
54280 Champenoux, France
5
EFI Atlantic, 69 Route dArcachon, 33612 Cestas, France
6
Forest Sciences Centre of Catalonia (CTFC-CEMFOR), Ctra. de St.
Llorenç de Morunys, km 2, 25280 Solsona, Spain
7
School of Biological Sciences, Royal Holloway University of
London, Egham, Surrey TW20 0EX, UK
8
Scion (New Zealand Forest Research Institute), 49 Sala Street,
Rotorua 3046, New Zealand
9
Scion (New Zealand Forest Research Institute), PO Box 29237,
Christchurch 8440, New Zealand
Curr Forestry Rep
DOI 10.1007/s40725-017-0064-1
Higher tree diversity translates into increased resistance to
disturbances as a result of ecological trait complementarity
among species, reduction of fuel and food resources for her-
bivores, enhancement of diversion or disruption processes,
and multi-trophic interactions such as predation or symbiosis.
To promote resistance, the selection of tree species with
different functional characteristics appears more important
than increasing only the number of species in the stand.
Trees with different levels of susceptibility to different hazards
should be intermixed in order to reduce the amount of exposed
resources and to generate barriers against contagion.
However, more research is needed to further improve asso-
ciational resistance in mixed forests, through a better under-
standing of the most relevant spatial and temporal scales of
species interactions and to optimize the overall provision of
ecosystem services.
Keywords Associational resistance .Associational
susceptibility .Biodiversity .Drought .Ecosystem services .
Fire .Fungal pathogens .Insect herbivores .Invasive species .
Mammalian browsers .Wind
Introduction
Forest ecosystems are frequently exposed to natural distur-
bances such as fires, windstorms and pest outbreaks that shape
forest structure and drive their dynamics [14]. While distur-
bances are essential for forest succession and biodiversity,
biotic and abiotic hazards may have negative impact on forest
health [5,6] and compromise the provision of ecosystem
goods and services [7].
Drought has negative effects on tree growth [8]. Carbon
starvation or hydraulic failure caused by severe drought can
lead to tree mortality [9]. Such drought effects have been
observed in forests worldwide [10]. Wind is another major
disturbance agent in forests [11]. For example, several storms
that occurred in 1999 in Europe caused windthrow and the
loss of 240 million m
3
of timber, representing approximately
60% of the annual European harvest [12]. In the USA, forests
across an area of 2.2 million ha were damaged by hurricanes
BKatrina^and BRita^in 2005 [13]. Forest fires are a global
phenomenon, affecting over 300 million ha annually [14].
They are very costly to society and the economy due to human
casualties and loss of property, expenses for suppression ac-
tivities [15], air pollution [16] and soil erosion [17].
Herbivory by mammals is an important source of tree dam-
age and mortality during the early stages of forest establish-
ment through browsing, stem breakage or bark stripping.
Even when this damage is moderate and does not kill the trees,
it often reduces tree growth and timber quality substantially
[18]. Insect herbivory causes similar levels of damageand can
even result in widespread tree mortality. More than 85
million ha of forests worldwide was reported to have been
affected by insect pests during the period from 2003 to 2012
[19]. Apart from the direct damage, insect herbivory affects
ecosystem functions such as primary production, carbon se-
questration, water and nutrient cycles, biotic interactions and
associated ecosystem services [7]. For example, massive bark
beetle outbreaks in western Canada resulted in tree mortality
equivalent to about one billion m
3
of wood [20]. Pathogens
causing diseases and dieback of forest trees can affect socio-
economic values provided by forests because of tree mortality,
reduced tree growth or a reduction in timber quality [21]. For
example, the root and butt rot basidiomycete fungus
Heterobasidion annosum s.l. has a significant impact on tim-
ber production, causing an estimated annual loss of 790 mil-
lion euros in Europe alone [22]. Similarly, sudden oak death in
California is predicted to result in damage exceeding 200 mil-
lion dollars [23]. In addition to native pests, invasive species are
a major increasing cause of disturbance in forests [2325]and
their economic damage alone can amount to billions of dollars
annually (e.g. [26]). Examples of invasive insect pests and
pathogens with particularly severe impacts include Dutch elm
disease, emerald ash borer and ash dieback, which are respon-
sible for the widespread and nearly complete death of elm and
ash trees in affected areas of North America and Europe [7], or
Phytophthora cinnamomi, a major threat to native forests and
theirbiodiversityinsouthwesternAustralia[27].
The frequency and severity of forestdisturbancesare likely
to increase, and there may be new combinations of distur-
bances as a result of global change and other anthropogenic
influences [28]. For example, since the mid-1950s, a trend of
increasing drought conditions has been reported for many
northern hemisphere areas [29]. Most climatic models predict
a decrease in summer precipitations across Europe [30]and
the USA [31], particularly at lower latitudes where areas af-
fected by drought are highly likely to increase [32]. There are
also serious concerns that wind damage will increase over the
twenty-first century because of more intense storms and in-
creasing susceptibility of forests (e.g. because of a reduction in
periods of frozen soil in Fennoscandia) [33]. Climatic factors
affecting vegetationmoisture and forest fuel accumulation are
also changing [34], and these are key factors that are likely to
lead to an increase in the number of large fires [35,36].
Populations of many mammalian herbivores (e.g. cervids)
have increased over the last few decades as a result of changes
in forest structure because of forestry practices such as clear
cutting, reduced mortality because of a lack of natural preda-
tors and a decrease in hunting pressure [37]. Global warming
may enhance the activity of forest pathogens [38], and increas-
ing drought could favour foliar pests and diseases [39].
Similarly, warming increases the population growth of many
pest insects [40] and may increase the number of generations
per year, thus resulting in more background herbivory [41]
and higher probability of outbreaks [42]. Rising temperatures
Curr Forestry Rep
may also remove environmental constraints that have previ-
ously limited the geographic distribution of certain pathogen
and insect species [4345],albeit other areas may become less
susceptible [46]. Increasing international trade and move-
ments of people have led to unprecedented rates of pest and
pathogen invasion (e.g. [47,48]), which are projected to in-
crease further in a globalized world [6,49,50]. Climate
change is also likely to facilitate further invasions by provid-
ing conditions conducive for the establishment of alien spe-
cies; for example, those originating from subtropical areas
may exacerbate their impacts in temperate areas [51].
Furthermore, because there are time lags of many years be-
tween the arrival of an exotic species and when populations
reach damaging levels across large areas (e.g. [52]), the im-
pacts of invaders are expected to increase even if no new
introductions were to occur.
The multiple hazards that threaten forests not only increase
concurrently but also interact and potentially synergize. For
example, more intense droughts trigger more frequent or more
severe fires as well as outbreaks of forest insects [21,5355]
and epidemics of forest pathogens [21,56] due to the increased
susceptibility of drought-stressed trees [39,57]. Storm damage
also leads to an increased risk of insect attack and fire because
affected trees are vulnerable to bark beetles [58,59]andpro-
vide an additional fuel load [60]. Bark stripping by mammali-
an herbivores makes trees more susceptible to fungal infection,
stem decay and wind damage [18,61], and decay caused by
root rot fungi in the lower part of the stem increases the sus-
ceptibility of trees to overturning by wind [62].
This situation points to the urgent need to develop new
forest management strategies that increase forest resistance
to multiple risks, both for socioeconomic and ecological rea-
sons [28]. While several recent reviews demonstratedthe pos-
sibility to reduce stand vulnerability through changes in silvi-
cultural treatments, including the choice of tree species (e.g.
[63,64]), a given silvicultural operation may have multiple,
sometimes opposing, effects on stand susceptibility to differ-
ent damaging agents. For example, thinning can improve in-
dividual tree vigour and increase individual tree resistance to
drought [65] or bark beetles [66] or prevent shoot diseases
[67]. However, thinned stands may also be more susceptible
to defoliators [68], root rot fungi [69] and initially, also wind
damage [70]. It follows that there are trade-offs and that few
forest management options simultaneously minimize the risks
from multiple types of hazard.
One generic approach for increasing forest resistance to
multiple damaging agents that has been discussed in the liter-
ature is increasing tree species richness at the stand level.
There is growing evidence that mixed forests could be bene-
ficial for a broad range of ecosystem functions and services
[71,72]. However, whether mixed forests are indeed more
resistant to all disturbances remains controversial. Even
though quantitative reviews suggest overall patterns of higher
resistance in mixed forests (e.g. [73]), there are many exam-
ples of lucky monocultures(i.e. pure forests that experience
little damage overall such as natural Nothofagus forests in
New Zealand) and unlucky mixtures(i.e. mixed forests that
were heavily damaged in spite of their diversity such as
Eucalyptus marginata forests in southwestern Australia fol-
lowing the invasion by P. cinnamomi)[74].
The term associational resistance(AR) was initially
coined to describe the greater resistance of plants against her-
bivores when surrounded by heterospecific neighbours (i.e.
adjacent plants of different species) as compared to plants
growing among conspecifics [75,76]. The opposite pattern
is termed associational susceptibility(AS). Several studies
reported associational resistance against insect herbivores
[77], mammalian herbivores [78,79] and foliar pathogens
[80,81]. We propose to extend this framework to resistance
against numerous biotic and abiotic stressors. Associational
resistance can thus be regarded as an emerging property of
assemblages of several tree species resulting in less damage
by natural disturbances.
The main objectives of this review were (1) to provide an
up-to-date review of the scientific literature addressing diver-
sityresistance relationships in forests for a broad range of
disturbances, namelydrought, wind storms, fire, mammal her-
bivores, insect pests, fungal diseases and invasive species; (2)
to identify common patterns of associational resistance (or
trade-offs) against biotic and abiotic hazards in mixed forests;
(3) to disentangle the ecological mechanisms underlying
these relationships and (4) to identify knowledge gaps
and research needs.
Patterns of Associational Resistance in Mixed Forests
Drought
Two types of approaches have mainly been used to test for
drought resistance in mixed forests, ecophysiological studies
(e.g. assessments of water use efficiency or transpiration) and
dendroecological methods (e.g. comparisons of tree growth in
dry vs. wet years or sites). Ecophysiological studies revealed
that the relationship between tree species diversity and forest
drought exposure varied with the forest biomes [82]. More
diverse forests tend to be less affected by intense droughts (i.e.
under severe drought conditions, water availability was higher
in diverse forest stands than in pure ones) in tropical regions
[8385] and in temperate regions [8689]. However, in forest
biomes with harsher climates, such as Mediterranean forests
[90,91]ormountainforests[82], there was no significant
effect of tree diversity on stand resistance to drought.
Moreover, in boreal forests, there was even greater drought
exposure with increasing diversity [92].
Curr Forestry Rep
Dendroecological studies focusing on tree growth in dry
years or at dry sites more often report positive effects of tree
species diversity ([9395], but see [96]). Recently, the long-
term productivity of various mixed forests in Europe was
demonstrated to be less affected by drought events than that
of pure forests [97]. However, another important finding is
that species-specific growth responses to drought are general-
ly asymmetric. Some tree species benefit from growing in
mixtures, like Abies alba [93]orFagus sylvatica [94], where-
as growth of the associated species does either not differ be-
tween pure and mixed stands under drought conditions or may
even be adversely affected. Therefore, differences in drought
responses between pure and mixed forests are probably due to
species identity effects ratherthan species diversity per se [98,
99]. Yet, there is no clear indication about which functional
groups of species (deciduous vs. evergreen, shade-tolerant vs.
shade-intolerant, etc.) would benefit more from species inter-
actions. Another general pattern is that when stand productiv-
ity increases with tree diversity, which is widely observed [71,
97,100], there is generally also an increase in water use effi-
ciency [89], i.e. an increase in the ratio of productivity to
transpiration. This is contrary to the common belief that more
productive forests use more water [101]. Therefore, the re-
sponse of tree species to drought in mixed forests is highly
variable, depending onthe composition of the mixture and the
environmental conditions, particularly edaphic features [99].
Based on the available evidence, identifying a general pattern
in the role of species diversity on stand-level drought resis-
tance is difficult at this time [89].
Fire
Forest susceptibility to fire greatly varies with tree species
identity and composition [102] because fire damage depends
on the capacity of a particular tree species to protect sensitive
tissues and therefore survive the fire [103,104]. In general,
foliage with high contents of resins and oils and low ash con-
tent, such as that of many conifers and eucalypts, is considered
to be more flammable than that of most deciduous
broadleaved tree species [105,106]. Therefore, pure conifer
forests are thought to be more sensitive to fire than
broadleaved forests [102], with mixed conifer and
broadleaved forests being intermediate, depending on their
species composition [107]. There is indeed a lot of evidence
from regions with frequent fire events that mixtures of coni-
fers and broadleaves are less prone to fire than pure conifer
forests (e.g. [108110]). In addition, fires in such mixed for-
ests tend to be of lower extent and intensity [111115].
Forest structure, characterized by the distribution of tree
age and size, is recognized as a very important factor control-
ling fire spread [114116], intensity [110], probability of fire
crowning [111] and ultimately, mortality rate at the stand level
[117••]. The effects of mixing tree species on forest
structure need to be considered to predict mixed forest
susceptibility or resistance to fire because different species
have different morphological characteristics. On the one
hand, multi-layer stands derived from species mixtures
may generate an undesirable ladder of fuelsthat increases
the probability of fire crowning, but on the other hand, they
may increase light interception, limiting the development
of understory vegetation, which decreases the intensity of
surface fires.
Mixing tree species may also change the structure of the
litter layer, its decomposition dynamics and hence, flamma-
bility. For example, in Californian mixed-conifer forests, the
flammability of litter mixtures from eight dominant tree spe-
cies was non-additive in the sense that it was higher than can
be expected from single-species litters owing to the
disproportionally large influence of the most flammable litter
component in mixtures [118]. However, there are so far too
few studies to derive any general conclusion regarding the
effect of mixing on litter flammability (e.g. [119].
Windstorms
There has been a long history of suggestions that wind dam-
age to forests can be reduced by the use of multi-species or
multi-structure forest stands. This thinking has emerged from
the observation that natural forest ecosystems, often charac-
terized by a large diversity of tree species and dimensions,
seem more resistant to storm disturbances [120]. Recently,
[121••] performed a meta-analysis comparing resistance to
windthrow in pure vs. mixed stands. Based on seven pub-
lished studies conducted in Europe, they demonstrated a sig-
nificant and positive effect of mixing tree species on resistance
against wind damage.
There is also increasing evidence for tree species differ-
ences in resistance to storms [122,123]. In particular, some
conifers species such as Picea abies are more susceptible to
wind damage due to more shallow rooting systems [124], i.e.
weaker anchorage and the presence of foliage throughout the
year, which increases the size ofthe crown area exposed to the
wind [125]. As a consequence, the admixture of broadleaved
species to conifers probably reduces the susceptibility of
mixed forests to wind damage [124,126]. In fact, a number
of studies in Europe have shown that mixed stands of conifers
and broadleaves are more resistant to windstorms than pure
conifer stands, with a significant reduction of overall dam-
age, irrespective of the tree species, suggesting a comple-
mentary effect [127131]. Similarly, [132] indicated that a
higher proportion of spruce in mixed stands increases the
risk of wind damage. However, there is little evidence that
the mixture of susceptible conifer species with less suscep-
tible broadleaves also reduces the windthrow damage to
the latter [133].
Curr Forestry Rep
Mammalian Herbivores
Several observational studies have shown relationships be-
tween tree species diversity and mammalian herbivory (e.g.
[134]), but such studies cannot separate causes and conse-
quences, for example, whether mammalian herbivory modi-
fied tree species diversity (through differential mortality) or
whether tree diversity affected mammalian browsing. The es-
tablishment of long-term forest diversity experiments during
the last two decades enabled more rigorous assessment of
forest diversity effects on mammalian herbivory. In the
Satakunta forest diversity experiment (Finland), [79]showed
contrasting effects of tree species richness on seedling damage
by voles (Microtus spp.) and moose (Alces alces). Vole dam-
age to tree seedlings was higher in monocultures than in
mixed stands, which corresponds to associational resistance.
In contrast, moose browsing tended to increase with the num-
ber of tree species in a stand (associational susceptibility) and
with the presence of the preferred tree species, birch, in a
mixture. Later, [135] found that both the percentage of trees
browsed by moose and the intensity of browsing per plot
increased with tree species richness, whereas browsing selec-
tivity decreased, with tree species being targeted more equally
in species-rich mixtures.
Mixed-species plots were twice as likely to be visited and
browsed by white-tailed deer than monocultures [136].
However, the intensity of deer damage was higher in mono-
cultures than in mixed-species plots. Tree seedling survival
was overall higher in tree mixtures than in monocultures in
the presence of deer. In particular, damage to highly preferred
tree species was reduced in tree mixtures, presumably because
the presence of less palatable species discouraged deer from
entering and spending more time within a mixed stand.
Because ungulate browsing mainly affects tree sapling sur-
vival, and hence natural regeneration of the stands, it is also
relevant to consider the effects of diversity of the understorey
vegetation. Many observational [137,138] and experimental
studies [139141] haveshown that unpalatable nurse plants or
shrub species protect tree seedlings or saplings from ungulate
browsing. In Australia, eucalyptus seedlings escaped brows-
ing by wallabies for a longer period when surrounded by un-
palatable native shrubs, resulting in higher survival [142]. To
our knowledge, there are no studies that have examined the
influence of tree mixtures on browsing by arboreal mammals.
Insect Herbivores
Several meta-analyses showed that, on average, a given tree
species is less damaged by insect herbivores when grown in
mixtures than in monocultures (i.e. associational resistance)
[77,143]. Recently, a large-scale study [144] focusing on
more than 200 mature forest stands in Europe demonstrated
that overall, herbivory damage to broadleaved species
significantly decreased with the number of tree species in a
mixture. This pattern of associational resistance was observed
across tree species and countries, irrespective of their climate.
However, the consistent general trend in these results hides the
large variability in insect species-specific response to mixed
forests [145] and several authors reported either neutral effects
of tree diversity or even associational susceptibility
[146149]. These differences probably result from differences
in herbivore specialization [77,143,148,150,151] since
generalist herbivores can benefit from a large array of host
plants. In a meta-analysis testing the effects of herbivore spe-
cialization, [143]showed that mixing tree species resulted in
significantly lower damage by monophagous (42%) and ol-
igophagous (15%) insect herbivores but had a neutral effect
on polyphagous species.
Variability in herbivory among species-poor mixtures is
therefore expected to be high and strongly influenced by the
identity and phylogenetic diversity of associated species.
Admixtures of broadleaved and conifer species provide better
associational resistance than mixtures of only conifer species
or only broadleaved species ([77], but see [145]). Similarly,
tree diversity triggered associational resistance to generalist
herbivores only when tree mixtures include tree species phy-
logenetically distant to the focal species [143]. However, as
tree species richness increases, both the probability of finding
suitable host tree species and the probability of recruiting po-
lyphagous herbivores might increase, leading to overall asso-
ciational susceptibility, as observed in a highly diverse tropical
forest [147].
Fungal Pathogens
Reduced damage in mixed forests, compared with single-
species forests, has been consistently observed for numerous
tree root pathogens. In North America, Armillaria ostoyae
root rot in susceptible conifer species decreased substantially
(50 to 100%) in mixed stands containing less susceptible hard-
wood species compared with pure conifer stands [152].
Likewise, alternating rows with less susceptible tree species
(cedar and birch) resulted in a reduced number and size of
Armillaria disease centres in Douglas fir and lodgepole pine
plots [153]. A large number of studies have been conducted to
elucidate whether mixing conifers (Pinus,Picea,Abies spp.)
with broadleaved tree species may decrease the spread and
damage caused by the decay pathogen H. annosum s.l.
through dilution effects (see [74,154] and references therein).
Most studies concluded that mixed stands are beneficial in
terms of reducing the incidence of damage from
H. annosum although the resulting effects were often rela-
tively small [154157]. Apparently, at least 20 to 30% of
evenly spaced trees of resistant species are needed in mix-
tures to reduce the decay frequency in susceptible conifers
substantially (e.g. [158]).
Curr Forestry Rep
The effects of tree diversity on forest resistance to foliar
pathogens are more variable. Recent results from a pan-
European study showed that foliar disease incidence at the
stand scale was only weakly related to tree diversity, and
whether the effect increased or decreased resistance depended
on the tree type [159]. For conifer species, foliar damage sig-
nificantly decreased with tree species richness (i.e. associa-
tional resistance), while there was a slight tendency for in-
creased damage in broadleaved species (associational suscep-
tibility). In temperate forest stands where tree species richness
was experimentally manipulated, overall foliar fungal infesta-
tion of Tilia cordata and Quercus petraea was decreased with
increasing tree species diversity of the neighbouring trees [81].
However, similar studies in other tree diversity experiments
found no such general effect [80,160]. Nevertheless, a more
general effect was observed in a plantation experiment in the
tropics, where damage caused by pathogens was lower or
equal in mixed-species plots compared to monocultures [161].
Generalist pathogens with a broad host range may also be
adversely affected by mixing tree species. In California, the
disease risk of Phytophthora ramorum was reported to be
lower in areas with higher tree species diversity, particularly
in mixed evergreen forests [162••].
It should be noted that the magnitude of associational re-
sistance to fungal pathogens appears to be larger when trees
with more contrasting traits are assembled, particularly in
mixtures of broadleaves and conifers (e.g. [81,152,153,
155,157,162••,163]). This is consistent with the results of
experimental inoculations in a tropical rain forest where the
likelihood of a pathogen infecting two tree species decreased
with the phylogenetic distance between these trees, a proxy of
their functional dissimilarity [164].
Invasive Species
A meta-analysis found a strong positive relationship between
the diversity of primary producers and invasion resistance, as
well as a negative relationship with invader fitness and invader
diversity [165]. However, most of the studies included in this
meta-analysis addressed effects on invasive primary pro-
ducers in grassland and aquatic ecosystems and none were
from forests.
Studies on forest resistance to plant invaders have pro-
duced conflicting results. Some studies (e.g. [166]) suggest
that biodiversity can enhance resistance to exotic plants. In
contrast, data from forest plots across the USA showed a pos-
itive correlation between native plant species richness and
exotic species richness [167,168]. There may not be a
causeeffect relationship between native and exotic species
richness. It is more likely that the richness of both native and
alien plants is controlled by the same factors, in particular,
greater habitat heterogeneity at large scales and increased re-
source availability at small scales. Indeed, in the eastern USA,
[168] found a negative effect of tree phylogenetic diversity on
invader establishment and dominance, i.e. a biotic resistance
to plant invasion. The type and structure of forests are other
possible controlling factors. In central Europe, a study com-
paring broadleaved and conifer monocultures with woodland
mixtures showed that broadleaved plantations were particular-
ly prone to plant invasions, compared to all other forest hab-
itats [169].
Regarding invasions by exotic insect herbivores, two stud-
ies in Europe documented negative relationships between the
abundance of invaders or the damage they caused and tree
species richness at the plot or stand scale, such that monocul-
tures were generally more affected [170,171••]. However, an
analysis of larger-scale patterns, at the county level in the
USA, found that the number of invasive forest insect pest
species was positively correlated with the number of tree gen-
era, suggesting that diverse forests were more easily invaded
by forest insects [172].
While these observations are not necessarily applicable to
stand-level processes, they suggest that forest invasibilityis
not simply a function of tree species richness but also depends
on the measure of invasion used and which trophic level is
being considered. At smaller scales (e.g. plot or stand), greater
plant diversity tends to reduce the ability of invasive plants to
become established. By contrast, a greater number of alien
insects can be expected to find host plants, although the out-
come of the mechanisms leading to associational resistance
may counter herbivore establishment and population growth
to damaging levels (see BInsect Herbivores^section). At larg-
er scales, positive correlations between native species richness
and exotic species richness predominate at both producer and
consumer levels and this has been interpreted as indicating
that greater tree species richness facilitates invasion.
However, these larger-scale patterns may obscure the outcome
of processes occurring at smaller scales.
General Findings
Despite the large variability of mixed forestsresponses to the
different types of natural disturbances, tree species diversity
appears to more often lead to associational resistance than to
associational susceptibility. However, the magnitude of AR,
and perhaps the amount of empirical evidence for AR, differs
among the types of disturbance. Based on the findings of our
review, the effect of tree species diversity on associational
resistance shows a gradient from weak or uncertain to strong
or consistent against hazards ranked in the following order:
drought, fire, windstorm, mammal herbivores, fungal patho-
gens and pest insects (native or invasive). This ranking paral-
lels, at least partly, the spatial scale at which these disturbances
normally occur and/or cause impacts (Fig. 1). Drought is driv-
en by continental or regional climate conditionsand can affect
large forest areas. Wind and fire are landscape-level
Curr Forestry Rep
disturbances, potentially affecting many forest stands, often
irrespective of their composition. Mammalian herbivores have
relatively large home ranges and can forage on several trees
within a stand. By contrast, within one generation, pathogens
and insect herbivores are often restricted in their ability to move
from one stand to another. This is particularly true for a number
of specialist species. Generalists and species that disperse eas-
ily (comprising a number of pests and diseases) can cover
larger areas during outbreaks. In such cases, their propagule
pressure may become so high that even diverse forests cannot
limit the spread (e.g. during mountain pine beetle epidemics).
However, there are only a few published studies on how asso-
ciational resistance varies with pest density [173,174].
An additional, not mutually exclusive, interpretation of this
pattern relates to hazard selectivity, i.e. the property of affect-
ing some tree species and not others (Fig. 1). Indeed, the cases
of large and positive effects of tree species diversity on asso-
ciational resistance of mixed forests are more frequently ob-
served against monophagous and oligophagous herbivores
(like specialized insects) or soil-borne pathogens than against
polyphagous herbivores (like generalist defoliators or mam-
mal browsers) or airborne pathogens. On the other hand, AR
is weaker or less frequently found in relation to drought, wind
and fire, all of which are not selectivedamaging agents, as
they can affect virtually all individual trees within a stand
irrespective of the species.
Another general finding is that the composition of mixed
forests (i.e. the identity and relative abundance of associated
species in mixtures) is more important than tree species rich-
ness per se to explain the resistance of mixed-species stands. It
often depends on the relevant traits of the participating
species and how they respond to stress and disturbance.
For some disturbances, the phylogenetic distance between
assembled species and, ultimately, the functional diversity
of species of which mixed forests are composed, are the
main drivers of AR. This is akin to many ecosystem pro-
cesses that are enhanced by plant diversity [175]. This is
particularly obvious for the association of broadleaved and
conifer species, which are often less damaged by both bi-
otic and abiotic agents, than pure forests of broadleaves or
pure forests of conifers.
Mechanisms of DiversityResistance Relationships
in Mixed Forests
The most obvious reason why mixed forests are likely to be
more resistant to disturbances than pure forest can be ex-
plained from a probabilistic perspective. Being composed of
several tree species with different functional traits, mixed for-
ests have a greater likelihood of containing at least some tree
species thatare more resistant to the various hazardsthey may
face, thus providing more opportunities to maintain forest
cover and to sustain basic ecosystem functions in the long
term, despite possible damage to other associated species.
This phenomenon of risk spreading is described in the insur-
ance hypothesis[176], which states that biodiversity insures
ecosystems against the impact of disturbances. The rationale is
that greater species richness and functional diversity increase
the likelihood that at least some species will survive and con-
tinue to function even if others do not. A key factor here is the
variability in species sensitivity or rapidity of responses (e.g.
Fig. 1 Putative relationships between the likelihood of associational
resistance (AR) or associational susceptibility (AS) of mixed forests to
natural disturbances, their spatial extent (horizontal axis), from wide (i.e.
region, km
2
) to narrow (i.e. single tree, m
2
), and their selectivity (vertical
axis), from low (i.e. irrespective of stand composition or structure) to high
(dependent on tree size and species). By selectivity, we mean the property
of affecting some tree species and not others. The intensity of colours
denotes the importance of AR (green colours)orAS(red colours)based
on empirical evidence
Curr Forestry Rep
asynchrony) to disturbances that is displayed in species-rich
communities [177]. Although mainly supported by observa-
tional studies [97,178] and modelling studies [179]onthe
stability ofmixed forestproductivity, the insurance hypothesis
is clearly relevant to mixed forestsresistance to major natural
disturbances as different tree species can display more or less
strong responses and variable recovery times to forest hazards.
However, beyond these probabilistic considerations, we sug-
gest four general mechanistic explanations of mixed forest
associational resistance and two for associational susceptibil-
ity. These can apply to all types of disturbance, as discussed in
the succeeding sections. Based on our interpretation of the
scientific literature, we further propose to rank the relative
relevance of these mechanisms in explaining mixed forest
resistance for the biotic and abiotic hazards addressed in
this review (Fig. 2).
General Mechanisms of Associational Resistance
to Natural Disturbances in Forests
Complementarity in Resistance Traits and Facilitation
Resistance to drought of mixed forests is thought to result
mainly from complementary below-ground processes, partic-
ularly root stratification [82,90]. When droughts develop,
deeply rooted species may experience less competition for
water when they are mixed with shallower rooting species,
compared with the level of competition among conspecific
neighbours in a pure forest. However, this mechanism will
be only effective until the entire soil profile has fallen dry.
Evidence of such below-ground stratification among tree spe-
cies has been found in temperate European forests (e.g. [88,
180,181]). Hydraulic lift could also take place in mixed
stands if a deep-rooting species takes up water and redistrib-
utes it to drier superficial soil layers. This case of facilitation
has been assumed to occur in particular mixtures [94].
Niche complementarity in water use may also occur in
mixed forests through reduced canopy interception of rain
water and increased stem flow through combinations of
species with different crown structures and leaf habits
(deciduous vs. evergreen) [93,182].
Better resistance to wind damage of mixed forests is likely
the result of the presence of more wind resistantspecies,
which will help to increase overall stability of the stand during
a wind storm by providing a framework of stable trees (i.e.
facilitation). In mixtures of species that differ in stem taper,
elasticity, crown density or root anchorage, and hence exhibit
different swaying characteristics [183], there may be more
mutual support through stand structure than in monospecific
stands of the participating species. In addition, the more stable
species may reduce damage propagation during a storm. This
occurs when an unstable or weak tree falls and creates a gap in
the forest, thereby increasing the wind loading on trees on the
downwind side of the gap, potentially leading to further dam-
age [184]. More stable trees within the stand can therefore act
as a way of arresting damage propagation and provide a more
stable framework for the stand. When the canopy of mixed
forests is multi-storied, the momentum absorption of the wind
appears to take place over a greater depth into the canopy and
this reduces the wind loading on the tallest trees [185]. In
some cases, slower-growing species will eventually die and
act as a self-thinning system that removes the dangers of arti-
ficial thinning when the canopy is opened up and immediately
increases wind loading [186]. There is also evidence that wind
loading on broadleaved trees is reduced in the winter, when
they have lost their leaves, and that an admixture of broad-
leaves to conifers may increase stand stability [130]. The
proximity of broadleaved trees may also modify the crown
architecture of neighbouring conifer trees, reducing their wind
surface area [124].
The resistance of mixed stands to fire mainly results from
the intermixing of tree species of varying levels of resistance
to fire through specific traits like thick bark, high growth rates,
pole-like form, rapid self-pruning, high insertion of lower
branches and low flammability of litter and foliage [187,
188]. As with wind resistance, the presence of the more fire-
Fig. 2 Preliminary assessment of the relevance of general ecological mechanisms explaining associational resistance (AR) of mixed forests to seven
types of natural disturbances
Curr Forestry Rep
resistant species helps to reduce the overall stand susceptibil-
ity to fire by restricting the spread of flames in horizontal and
vertical directions.
Because biological invasions typically begin with an initial
small founder population in one location, the mechanisms that
ultimately explain the relative invasibilityof habitats are those
that operate at the plot or stand scale. The availability of un-
occupied niches is a key driver, but whether mixed forests
provide fewer or more niches is a function of the trophic level
of invaders. In the case of plants, it is generally assumed that
habitats with greater plant diversity provide fewer vacant
niches for invasive plants (e.g. [189]). In the case of herbi-
vores such as plant-feeding insects and plant pathogens, great-
er plant diversity is likely to result in a greater variety of niches
(e.g. more potential host plants), potentially leading to in-
creased establishment opportunity and invasibility (e.g.
[172]), although plant diversity and the density of particu-
lar niches are inversely related which would be expected to
decrease invasibility.
Reduction of Fuel/Food Resources
In mixed stands, the more stable tree species may reduce wind
damage propagation during a storm. This occurs when an
unstable or weak tree falls and creates a gap in the forest,
thereby increasing the wind loadingon trees on the downwind
side of the gap, potentially leading to further damage [184].
There are thus fewer susceptible trees in mixed forests to
feedthe windthrow [121••,190]. The same appears to apply
regarding fire resistance of mixed forests when there is a great-
er proportion of resistant tree species than fire-prone species
thus reducing the risk to fuelthe fire [113,117••]. In addi-
tion, mixing of species with different shade tolerances, in par-
ticular, admixing of species with high shade tolerance to light-
demanding species, may reduce the development of
understorey and hence levels of fine fuel.
Greater tree diversity commonly results in a lower density
of suitable host species for herbivores and pathogens (and
reciprocally, a higher amount of less favourable, or non-host
species). The resource concentration hypothesis [75]predicts
that dense stands of the same tree species would recruit more
specialist herbivores than less dense stands, because they are
easier to locate in the landscape and provide more resources
for building up populations. This hypothesis received impor-
tant empirical support from recent studies on insects [151,
191194]. However, whether herbivory will increase (or
decrease) with an increase in host tree density depends on
the relative importance of concentration effects (where in-
creased herbivore density results in more damage, e.g.
through better reproduction) vs. dilution effects (where
herbivores distributed across more trees result in reduced
per capita infestation rates) [68,195197].
The resource concentration hypothesis also suggests that
pest and disease risk is reduced with increasing host diversity
due to reduced host density and increased distance between
host trees, thus affecting the herbivore or pathogenhost en-
counter and transmission potential [198]. For example, several
forest insects are wind-dispersed, such as the young larvae of
the budworm Choristoneura fumiferana, that show higher
survival in pure stands of their host trees than in mixed stands
due to the reduced risk of landing on a non-host [199], thus
resulting in more defoliation of balsam fir in pure stands [200].
Such a dilution effect is also particularly relevant for patho-
gens, as they are often dispersed through passive transmission.
Phytophthora lateralis infection of cedars, for example, was
found to be related not only to host density at a site but also to
the distance between inoculum source and the closest tree
[201]. Hantsch et al. [80] observed a reduction in oak powdery
mildew in mixed plots irrespective of the identity of
heterospecific neighbours, suggesting that associational resis-
tance was mainly driven by host dilution, i.e. a decrease of
host tree density and spread opportunity for pathogen propa-
gules. Similarly, [152] demonstrated that conifer tree mortality
caused by A. ostoyae was inversely related tothe proportion of
non-host broadleaves in mixtures as a result of increasing
spacing between host trees.
Given that higher tree diversity in a stand usually results in
lower average density per tree species, the reduced concentra-
tion and availability of particular host plant species in forest
mixtures are also likely to reduce the probability of establish-
ment of exotic and invasive species, according to the resource
availabilityhypothesis [202].
Reduced Host/Target Tree Accessibility Through Disruption
or Diversion
The presence offire-resistant trees in a mixture may provide a
physical barrier, limiting flame propagation, thus preventing
ignition of neighbouring less resistant trees [203]. Likewise,
the presence of shrubs or tree saplings with good defence
against mammalian herbivores can prevent damage of nearby
focal young trees [137,138,140,204207].
Non-host trees may also reduce the physical and chemical
apparency of host trees to insect herbivores, making them less
likely to be found. For instance, tall heterospecific neighbours
may physically hide smaller host trees from insect defoliators
[151,192,208,209]. Non-host trees may also release volatiles
interfering with insectshost-searching behaviour [210213]
or triggering specific defences towards them [214,215].
Importantly, reduced host tree density also comes with a de-
crease in the amount of olfactory and visual host cues, just as
higher non-host density may increase the amount of confusing
or repelling non-host cues [216,217]. These processes rely
on contrasting traits among tree species, which can explain
why associational resistance to insect herbivores increases
Curr Forestry Rep
with the phylogenetic distance between tree species that
make up forest mixtures [143].
Reduced damage by root pathogens in mixed tree stands
suggests that non-host species may also act as a barrier for
further pathogen spread via root contact in the soil [152,
153]. Studying the root rot fungus, Phellinus sulphurascens,
[218] found aninverse relationship between tree diversity and
the rate of mycelium growth in soil, indicating that mixed
stands may reduce the rate of spread.
The attractantdecoy hypothesis posits that herbivory on a
focal plant in a mixed stand can be reduced when it is
surrounded by more attractive or palatable neighbours,
through a diversion process (reviewed in [212]). Lower inten-
sity of damage by mammalian herbivores in mixed-species
stands could be due to selective browsing on competitive
dominants. For example, deer preferentially consumed the
most productive and competitive species, which enhanced
the survival of subdominant species. But, as deer browsing
in mixtures was not very intense, this was not enough to kill
the highly preferred species, leading to higher seedling surviv-
al overall [136]. Likewise, tree species were targeted by
moose more equally in species-rich plots (lower within-plot
selectivity) compared with species-poor plots where moose
predominantly target preferred species such as pine [135].
Polyphagous insect herbivores probably also behave like
mammal herbivores in mixed forests [73]. Focal tree species
could be protected from insect herbivory by the presence of
associated and more palatable tree species that would be
exploited first. For example, the presence of more palatable
shrubs or trees in the inter-row of eucalyptus plantations re-
sulted in lower infestation by Amblypelta cocophaga [219]
and Chrysophtharta bimaculata [220]. However, using the
attractantdecoy hypothesis as a basis for forest management
should be considered with caution as the attractant species
may eventually turn into a sourceof herbivores and pathogens
which may spill over onto associated species as their popula-
tion density increases [221].
Multi-trophic Interactions Enhancing Symbiosis
and Predation
A potential mechanism behind improved resistance of mixed
forest stands to drought is the positive influence of tree species
richness on mycorrhizal fungi [222], which are known to im-
prove tree water uptake [223].
There might also be benefits of tree species mixtures
against wind damage on soils with limited nutrient availabil-
ity, where the favourable mycorrhizal activity of the nurse
species promotes faster growth [224] and allows the dominant
species to grow tall without compromising the root and stem
diameter allocation necessary for tree stability.
Natural enemies of insect herbivores such as parasitoids,
spiders, insectivorous birds and bats are key components of
pest regulation in forest ecosystems. The enemies hypothesis
[75] states that the abundance and richness of predators and
parasitoids increase with plant diversity. Because herbivores
may spend more time to forage for food in mixtures than in
monocultures, they may be more at risk at predation (the
movement risk hypothesis, [225]). Although several studies
confirmed that abundance and diversity of predators and par-
asitoids can increase with tree diversity [226231], it is still
controversial whether this translates into a more effective her-
bivore suppression [232,233]. A greater abundance and di-
versity of enemies is expected to provide a better topdown
control of herbivores, but the opposite may occur if greater
diversity of enemies results in more intraguild predation [234,
235]. The positive relationship between the diversity of ene-
mies and herbivore suppression may also be due to high pop-
ulation density of herbivores with patchy distribution and spe-
cialization of different enemies feeding on different life stages
of the same prey [235,236].
It has also been suggested that mixed forests are more re-
sistant to fungal diseases because they can accommodate an-
tagonistic microorganisms. For example, E. marginata die-
back was less prevalent inmixed forests with Acacia pulchella,
presumably because the rhizosphere of A. pulchella contained
bacteria and actinomycetes that were able to inhibit mycelial
growth and spore production of the dieback pathogen
P. cinnamomi [237]. Likewise, [238] showed that bacteria
from soils under birchDouglas fir mixtures have inhibitory
effects against the decay fungus A. ostoyae.
One of the main reasons for the success of alien herbivores
[239] relates to the enemy release hypothesis[240], which
states that herbivores escape their natural enemies because
they have not followed them into newly colonized areas. It
is thus expected that a large diversity of generalist predators,
driven by higher tree diversity, would lead to a stronger regu-
latory effect on naïve and exotic prey, than on native ones.
This was observed in the Mediterranean island of Corsica
where a native generalist predatory bug occurs in mixed
Corsican pine and maritime pine forests but not in pure mar-
itime forests, and there is compelling evidence that this is the
reason why pure maritime pine forests were more invaded by
Matsucoccus feytaudi, a non-native scale insect [170].
Three Facets of Tree Diversity That Can Drive the Four
Mechanisms of Associational Resistance
Tree species richness at the stand level leads to three non-
exclusive changes in the amount or diversity of resources that
may drive the impacts of natural disturbances. Tree diversity
can (i) increase resourceheterogeneity through an assembly of
tree species with different traits; (ii) reduce resource quantity
through replacement of preferred/susceptible host trees (spe-
cies A) with trees from unsuitable species and (iii) limit re-
source connectivity by interspacing host/target trees (of
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species A) with heterospecific trees. Each of the three
facets of resource change in mixed forests may trigger
the proposed general mechanisms underlying associational
resistance (Fig. 3).
Greater resource heterogeneity mainly increases positive
complementarity effects among tree species with contrasting
traits and the likelihood that alternative prey and/or suitable
habitats benefit to natural enemies, which are able to control
pests, or to fungal symbionts, which can improve water and
nutrient uptake.
The lower relative amount of the focal host species in a
mixed stand reduces resource quantity in terms of food (for
herbivores) or fuel (for wind and fire), thus limiting the ability
of disturbance to build up to high levels.
Increasing the distance between trees of focal host species
reduces resource connectivity and is likely to limit focal tree
access and thus exposure to disturbance (e.g. spread of
pathogens).It is noteworthy that reduction of both resource
quantity and connectivity can be obtained with low levels
of tree species richness (even as low as two species,
Fig. 3). It also suggests that the spatial arrangement of
individual trees from different species can greatly influ-
ence the magnitude of AR.
General Mechanisms of Associational Susceptibility
to Natural Disturbances in Forests
Competition for Resources
Because mixed forests are often more productive than tree
monocultures (overyielding) [241], greater stand basal area
may result inincreased water use [101]. This may make mixed
forests more prone to drought effects [89]. Faster growth and
higher stand density in more productive mixed forests could
also lead to higher sensitivity to wind damage because of
increased height growth, higher canopy roughness and chang-
es in tree allocation patterns (e.g. [70,133]). In addition,
below-ground competition might lead to shallower root sys-
tems in one or more species. For example, root systems of
P. abies were shallower when the species was mixed with
F. sylvatica than in monospecific stands [242].
A greater abundance and diversity of natural enemies
accommodated by mixed forests may, in some cases, result
in competition for prey resources and stronger intraguild
predation [234,235], thus reducing their ability to control
insect herbivores.
Spillover, Contagion and Alternating Between Host Trees
The presence of highly flammable tree species may translate
into a potential increase in damage to less flammable tree
species grown in mixed forests through a contagion process
[243]. The non-additive effects of mixing fuels on flammabil-
ity [118,119,244] may further enhance this effectas the most
flammable fuels appear to be the main driver of fire charac-
teristics. In addition, multi-layer mixed forest may provide a
ladderstructure that could result in increased risk of crown
fire. In the case of tropical rain forests, the introduction of fire-
tolerant species can modify the forest microclimate favouring
the occurrence of fires [245].
Under strong gusts, trees from less wind-resistant species
may fall and then cause subsequent wind damage in
neighbouring trees, possibly leading to a domino effect. The
Fig. 3 Correspondence between three facets of forest stand diversity and
four putative mechanisms of associational resistance. Increasing tree
diversity by converting monoculture of focal tree species A (green
squares for A trees) into species mixture leads to (1) increased resource
heterogeneity (when several tree species are mixeddifferent colours of
squares represent different species), (2) reduced quantity of species A per
area (due to presence of species B, yellow) and (3) increased isolation
between trees of species A (due to interspersed trees of species B, yellow).
Increased resource heterogeneity mainly enhances biotic interactions
(symbiosis, predation) through provision of alternative hosts and
increases the likelihood of assembling species with complementary
resistance traits. Reduced target tree quantity limits fuel or food
availability. Higher focal tree isolation enhances host finding disruption
or diversion
Curr Forestry Rep
potential occurrence of such a phenomenon has not been well
studied, but it has been assessed in sprucebeech mixed for-
ests where the results indicated that itwas not a problem [130].
Associational susceptibility to herbivores (i.e. more herbi-
vore damage on a given species surrounded by heterospecific
neighbours) has been observed with large mammals (e.g.
moose [135]) and polyphagous insects [147,149]). Three
main mechanisms may explain this negative diversity effect.
First, generalist herbivores with a wide host range can build up
their populations on preferred hosts but then spill over onto
neighbouring less suitable host trees when the resources pro-
vided by the former are becoming sparse [221]. Second, po-
lyphagous herbivores may take advantage of diet mixing
whereby their feeding on diverse food resources may provide
a better balance of nutrients, while potentially reducing expo-
sure to toxic compounds [246]. For herbivores, the balance
between attractantdecoy and spillover effects likely depends
on herbivore density, which remains to be explored [174].
Third, mixtures of closely related species, given their shared
evolutionary history, may be seen by pests and pathogens as
homogeneous resource patches and may be as attractive and
susceptible as monocultures [143,247].
Increasing tree diversity may also lead to amplification
effects on pathogens [198], which can occur if an added tree
species in the mixture is important for completing the patho-
genslife cycle. This is the case for many rust fungi, for ex-
ample. The susceptibility of Scots pine stands to pine-twisting
rust (Melampsora pinitorqua) was shown to be explained by
the presence and number of aspen, the alternate host of the
rust, in the stand [248].
Conclusion and Future Research
Many more observational and experimental studies are needed
to better ascertain the generality of patterns of forest diversity
resistance relationships proposed here and better decipher the
underlying mechanisms. We identified four main research av-
enues that are particularly in need of further work.
Metrics of Biodiversity
In this review, we mainly focused on tree species diversity and
the diversity of tree species traits. Functional traits permit a
relatively simple quantification and mechanistic interpretation
of tree diversity effects on process rates, including resistance
to disturbances [249]. For example, certain leaf traits deter-
mine resistance to pathogens and herbivores or the flamma-
bility of litter. There are also most probably below-ground
traits (e.g. root architecture) that are highly relevant to resis-
tance patterns (to drought, wind and root pathogens, for ex-
ample), but these are rarely measured.
Furthermore, recent studies have shown that relationships
between biodiversity and ecosystem functioning can partly be
explained byintraspecific variability and phenotypic plasticity
of traits [250,251]. Interactions among adjacent trees of dif-
ferent species in mixed forest may explain effects of variation
in species-specific traits, notably those involved in tree growth
and palatability. For instance, leaf nutrient content and anti-
herbivore defences were shown to differ between monocul-
tures and mixtures [252255]. However, how far such indirect
trait-mediated effects of tree diversity are relevant to produc-
tivity has to be better evaluated.
The genetic diversity within a tree species can have a large
impact on susceptibility to pests and pathogens [6,256]. But
whether the association of multiple tree genotypes (e.g.
clones and full-sib families) may provide a similar level
of resistance to natural disturbances as the mixing of tree
species remains to be studied (e.g. [174,247,252,257,
258] for resistance to herbivores).
Spatial Scales of DiversityResistance Relationships
The hierarchical framework of species assembly rules [259]
states that communities are shaped by successive filters, oper-
ating at different spatial scales, including regional species
pools, habitat area and isolation, local environmental con-
straints and biologicalinteractions. These nested filters should
also influence the functional diversity of local communities
[260] and associated ecosystem services. It is therefore impor-
tant to better understand at which spatial scales the effects of
forest diversity on resistance to disturbances are operating. For
example, the propagation of damage from wind storms and
fires is not only affected by forest stand structure and compo-
sition but also by forest landscape heterogeneity, which can
either provide a succession of barriers (e.g. resistant patches of
particular habitats) or increase the connectivity of susceptible
land cover types (e.g. spatial arrangement of fuel, [261]).
Likewise, herbivores (especially large mammals) select habi-
tat and resources in a hierarchical spatial manner [262].
Herbivores may decide to enter a patch of forest habitat de-
pending on certain characteristics of habitats and adjacent
patches, a process operating at the landscape scale. By con-
trast, mechanisms of associational effects, like reduction of
apparency of the focal plant or induction of chemical defence
[76], typically operate at smaller scales, for example, among
neighbouring plants [142]. Within forest stands, the spatial
configuration of trees of different species may also be critical.
Stokes and Stiling [263] showed that associational resistance
to insects was stronger when trees of different species that
shared herbivore enemies were closer to each other because
this facilitated the spillover of parasitoids. The transmission
of fungal pathogens is dependent not only on tree spacing
within stands (e.g. [152]) but also on the configuration of
Curr Forestry Rep
the surrounding landscape which interacts with large-scale
dispersal processes [264].
Temporal Dimensions of DiversityResistance
Relationships
Temporal dynamics is a largely overlooked dimension of di-
versityresistance relationships. Whether these relationships
are present over the longer term or only temporarily is an
important question that needs more investigation. Forest trees
are long-lived organisms that are exposed to impacts of mul-
tiple stresses over long periods (many decades), and these can
modify their resistance through ontogenic [265]orepigenetic
processes [266], plasticity [267] or structural changes [268].
Similarly, stands are managed over forestry cycles of many
decades during which a succession of disturbance events can
affect both their productivity and also their structure and com-
position, thus in turn modifying their susceptibility to subse-
quent disturbances. Therefore, it is important to better under-
stand how tree diversity may reduce forest damage in the long
term, at least for a forest rotation, and to assess the overall
benefit at the time of harvesting.
Temporal variation is another important aspect of tempo-
rality. While an increasing number of studies confirm the pos-
itive influence of forest diversity on the stability of provision-
ing services, particularly on primary productivity [97,179],
the effects of tree diversity on forest resilience to natural dis-
turbances are less well-understood [133,269]. Reducing the
time of recovery from disturbance is as important for the func-
tioning of forest ecosystems as limiting immediate impacts. A
better understanding of diversityresilience relationships re-
quires long-term ecological studies that enable consideration
of several successive disturbances (e.g. recurrent fires and
cyclic epidemics) or the incorporation of risk factors in forest
growth and dynamics models [270].
Trade-Offs, Synergies and Compromises
Tree diversityresistance relationships are complex, and re-
sponses to different types of disturbances that occur over the
life of a tree may vary, including interactions that can be dif-
ficult to predict. For example, recent studies demonstrated that
mammalian herbivory can affect tree diversity effects on in-
sect herbivores. Moose browsing in mixed stands altered the
direction of tree diversity effects on insect herbivory on birch
with unbrowsed trees experiencing associational resistance to
chewing insect damage while browsed trees suffered more
damage from insect chewing in mixed stands [271].
Similarly, diversity effects on insects can have cascading ef-
fects on pathogens, and vice versa. This is because insect
herbivores and pathogens commonly co-occur within the
same trees, eliciting direct and indirect plant-mediated inter-
actions [272]. At the stand scale, the presence of broadleaved
species in pine forests may reduce the impact of herbivores,
although certain tree species may exacerbate impacts of
heteroxenic pathogens like rusts [248]. There are therefore
many opportunities for either synergies or trade-offs among
tree diversity effects on successive or simultaneous hazards. A
more holistic approach is needed in order to design mixed
species forests that are more resistant to multiple hazards
while minimizing the risk of trade-offs. Better compromises
are likely to result from the mixing of a large number of tree
species, which should increase the occurrence of associational
resistance to multiple disturbances (i.e. the insurance hypoth-
esis) or from the mixing of particular tree species allowing
better trait complementarity. However, it shouldbe recognized
that forest managers are at least as interested in improving
ecosystem services other than regulating services (e.g. natural
hazards regulation), such as improving provisioning (e.g. pro-
ductivity) orsupporting services (e.g. habitat for biodiversity).
Furthermore, managers are also concerned that the cost of
forest management does not threaten their economic viability.
While mixed forests will certainly necessitate additional
considerations and are likely to increase the costs of man-
agement and harvesting [273], their improved adaptive ca-
pacity may still result in overall improved financial secu-
rity and net benefits [126,274].
Despite the fact that an increasing number of empirical
studies demonstrate that mixed forests can deliver many eco-
system services to a higher level than pure forests (e.g. [71,
72]), including regulating services (this review), only a tiny
proportion (less than 0.1%) of todays plantation forests
worldwide are made of tree species mixtures [275]. At a time
when planted forests continue to expand, potentially
representing ca. 20% of the total forest area by the end of
the century [276], more efforts should be made to develop
new mixed planted forests [277]. Obviously, it is essential to
support this endeavour with interdisciplinary research. The
collaboration of forest ecologists, silviculturists and econo-
mists is needed to determine the optimal design, species com-
position and management of mixed forests that are most likely
to provide a good balance among these different objectives
while improving cost-effectiveness. The use of multi-criteria
analyses would provide a good basis for the development of
such decision-making tools [278].
Acknowledgements This review has been conducted with the support
of the IUFRO (International Union of Forest Research Organizations)
Task Force on Biodiversity contribution to ecosystem services in man-
aged forests. The ideas developed in this review have also been
discussed during a workshop organized by J. Bauhus within the frame
of the FunDivEUROPE project, funded by the European Union Seventh
Framework Program (FP7/2007-2013), under the grant agreement no.
265171. We are grateful to the Ramon y Cajal Program from the
Spanish Ministry of Science and Education and the CERCA
Programme of the Generalitat de Catalunya for supporting the work of
Dr. Gonzalez-Olabarria. Contributions by EB were supported by MBIE
core funding (C04X1104) to Scion and the Better Border Biosecurity
Curr Forestry Rep
collaboration (http://www.b3nz.org), and MBIE contestable funding
(C09X1307) to the BESTprogramme. J. Boberg was supported by
Future Forestsa multi-disciplinary research program supported by the
Foundation for Strategic Environmental Research (MISTRA).
Compliance with Ethical Standards
Conflict of Interests Drs Jactel, Bauhus, Bonal, Castagneyrol,
Gardiner, Gonzalez-Olabarria, Koricheva, Meurisse and Brockerhoff de-
clare no conflicts of interests.
Boberg declares compensation from Future Forests, a research pro-
gram supported by the Foundation for Strategic Environmental Research
[MISTRA] in Sweden.
Human and Animal Rights and Informed Consent This article does
not contain any studies with human or animal subjects performed by any
of the authors.
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