Download Climate change and multitrophic interactions in soil: the primacy of

Global Change Biology (2012) 18, 2111–2125, doi: 10.1111/j.1365-2486.2012.02667.x
REVIEW
Climate change and multitrophic interactions in soil: the
primacy of plants and functional domains
S U K U M A R C H A K R A B O R T Y * , I R E N E O B . P A N G G A † and M A R G A R E T M . R O P E R ‡
*CSIRO Plant Industry, Queensland Bioscience Precinct, 306 Carmody Road, St. Lucia, Queensland 4067, Australia, †Crop
Protection Cluster, College of Agriculture, University of the Philippines Los Baños, College, Laguna 4031, Philippines, ‡CSIRO
Plant Industry, Underwood Avenue, Floreat, Western Australia 6014, Australia
Abstract
Soil multitrophic interactions transfer energy from plants as the predominant primary producer to communities of
organisms that occupy different positions in the food chain and are linked by multiple ecological networks, which is
the soil food web. Soil food web sequesters carbon, cycles nutrients, maintains soil health to suppress pathogens,
helps plants tolerate abiotic and biotic stress, and maintains ecosystem resilience and sustainability. Understanding
the influence of climate change on soil multitrophic interactions is necessary to maintain these essential ecosystem
services. But summarising this influence is a daunting task due to a paucity of knowledge and a lack of clarity on the
ecological networks that constitute these interactions. The scant literature is fragmented along disciplinary lines, often
reporting inconsistent findings that are context and scale-dependent. We argue for the differentiation of soil multitrophic interactions along functional and spatial domains to capture cross-disciplinary knowledge and mechanistically link all ecological networks to reproduce full functionalities of the soil food web. Distinct from litter mediated
interactions in detritosphere or elsewhere in the soil, the proposed ‘pathogen suppression’ and ‘stress tolerance’ interactions operate in the rhizosphere. A review of the literature suggests that climate change will influence the relative
importance, frequency and composition of functional groups, their trophic interactions and processes controlling
these interactions. Specific climate change factors generally have a beneficial influence on pathogen suppression and
stress tolerance, but findings on the overall soil food web are inconsistent due to a high level of uncertainty. In addition to an overall improvement in the understanding of soil multitrophic interactions using empirical and modelling
approaches, we recommend linking biodiversity to function, understanding influence of combinations of climatic factors on multitrophic interactions and the evolutionary ecology of multitrophic interactions in a changing climate as
areas that deserve most attention.
Keywords: biological control, carbon sequestration, endophyte, mycorrhiza, plant growth promotion, rhizosphere, soil borne
plant pathogens, soil food web, soil health, suppressive soil
Received 9 January 2012; revised version received 6 February 2012 and accepted 10 February 2012
Introduction
Soil multitrophic interactions involve plants, herbivores, predators, endophytes, pathogens, decomposers
and other functional groups that occupy different positions in the food chain and perform vital functions to
deliver ecosystem services that support life and cultural
services not associated with material benefits [United
Nation’s Millennium Ecosystem Assessments, (MEA,
2005)]. As the dominant primary producer in terrestrial
and soil ecosystems, plants are the main source of food
for all organisms at higher trophic levels, such as herbivores at level 2, predators at levels 3 and beyond. Soil
multitrophic interactions mediate > 80% of processes to
Correspondence: Sukumar Chakraborty, tel. + 617 3214 2677,
fax + 617 3214 2900, e-mail: [email protected]
© 2012 Blackwell Publishing Ltd
sequester carbon, decompose organic matter, cycle
nutrients, maintain soil fabric and structure and regulate the population of pest and pathogens (Barrios,
2007; Kabouw et al., 2011). Therefore, it is essential to
determine whether climate change will adversely
influence multitrophic interactions to affect ecosystem
services.
The estimated number of species in soil is 100 000 for
protozoa; 500 000 for nematodes; 7000 for earthworms;
and a significant proportion of the 1.5 million fungal
species (Susilo et al., 2004; Coleman & Whitman, 2005).
The number of bacterial species range between 6000 and
50 000 (Van Der Heijden et al., 2008). With 55–98% of the
total biodiversity on Earth (Beed et al., 2011), few other
ecosystems can match the size, complexity or the biodiversity of the soil biota. The complex interactions involving this biodiversity (McCann, 2007) in a heterogeneous
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2112 S . C H A K R A B O R T Y et al.
soil environment (Wolfe & Klironomos, 2005; Wardle,
2006) makes soil multitrophic interactions scale-dependent (Van Der Putten et al., 2004) and difficult to understand (Van Der Putten et al., 2001; Pritchard, 2011). This
is reflected in the limited literature on soil multitrophic
interactions (De Román et al., 2011; Johnson et al., 2011;
Van Dam & Heil, 2011). The complexity also obscures
understanding of essential processes such as the temperature sensitivity of soil carbon decomposition and feedbacks to climate change, despite much research
(Davidson & Janssens, 2006; Conant et al., 2011).
While Earth’s climate has always changed over time,
since the industrial revolution, human-induced CO2
emission has risen from 280 mg kg 1 in 1750 to 379
mg kg 1 in 2005. The radiative forcing due to greenhouse gas emissions has increased global surface temperatures by 0.74 °C over the past century and this is
projected to continue by between 0.15 and 0.3 °C per
decade, depending on the emission scenario (IPCC,
2007). Recent observations indicate that between 2000
and 2007 emissions have risen by 3.4% per year,
exceeding almost all projections from the Intergovernmental Panel on Climate Change (Raupach & Canadell,
2010). Rising sea levels, shrinking glaciers and
increased rainfall in the middle and high latitudes of
the Northern Hemisphere but a decrease over the subtropics are among other projected changes. Heat waves
and heavy precipitation may become more frequent
and tropical cyclones may be more intense in the 21st
century (IPCC, 2007).
Historically, reduced agricultural production under
cooling has caused price inflation, famine and war,
reducing human populations (Zhang et al., 2007). The
‘fertilization effect’ of rising CO2 concentration can
increase crop biomass and grain yield (Ainsworth &
Long, 2005), potentially increasing food production. But
yield increases are moderated by interactions, including
multitrophic interactions controlling water and nutrient
availability, and pest and disease outbreaks. These and
other biophysical elements will combine with social and
economic factors to determine food security under
future climates (Chakraborty & Newton, 2011).
For individual species, rising CO2 and temperature
will modify its biology and shift its geographical range,
and some will face extinction if these rises continue
beyond their tolerance limit. But influences on individual species cannot be used to project influences on multitrophic interactions, which involve many species/
functional groups linked by networks of ecological
interactions that operate simultaneously (Olff et al.,
2009). With more than one species carrying out the
same function, there is redundancy. This richness of
species that underpins soil resilience (Wakelin et al.,
2010), also contributes to the variability inherent in
most studies on multitrophic interactions. Despite proposed frameworks for community interactions (Hassall
et al., 2006; Gilman et al., 2010) very little published
works have considered the influence of climate change
on soil multitrophic interactions. Reviews have mostly
covered some theoretical (Newman, 2007) and empirical aspects (Van Der Putten et al., 2004; Blankinship &
Hungate, 2007; Brussaard et al., 2007; Pritchard, 2011)
of climate change and multitrophic interactions.
This review argues for a clear differentiation of multitrophic interaction networks that comprise the ‘amorphous’ soil food web and a renewed focus on the
primacy of plants as the mediator of climate change
impacts on soil multitrophic interactions. We recognise
and describe two distinct spatial and functional
domains under ‘stress tolerance’ and ‘pathogen suppression’ as components of soil food web. We briefly
review recent literature on the influence of climate
change on these multitrophic interaction networks to
synthesise cross-disciplinary knowledge. We recommend four major lines of enquiry to help guide future
research. The review aspires to stimulate debate and
discussion rather than offer an exhaustive review of literature on the potential influence of climate change on
soil multitrophic interactions.
Multitrophic interactions in soil: the need for clear
differentiation of multitrophic interaction networks
Microbial activity does not occur uniformly throughout
the soil but in ‘hot spots’ of specialised ecological
niches like the rhizosphere and detritosphere (environment surrounding decomposing litter), and physical,
chemical and biological heterogeneity support and
maintain these niches. Functional dynamics of biological processes can be better understood by focusing on
‘hot spots’ (Blackwood & Paul, 2003; Wakelin et al.,
2010).
The literature mostly ignores the networks of ecological interactions comprising soil food web that operate
simultaneously to perform specific functions. Classifying soil food web according to energy channels (Moore
et al., 1988; Holtkamp et al., 2008), trophic controls
(Scherber et al., 2010) or size-based templates (Olff
et al., 2009) have not improved understanding. On the
other hand, disciplinary research in ecology, soil microbiology, plant pathology, and others, offers understanding of specific aspects of soil multitrophic
interactions but overlooks important processes and
mechanisms that operate at different scales. Food webs
are more than the sum of their trophic elements (Cohen
et al., 2009) and the failure of mathematical models to
predict climate change impacts on soil food web (Smith
et al., 1998) is a reflection of knowledge gaps. This has
© 2012 Blackwell Publishing Ltd, Global Change Biology, 18, 2111–2125
C L I M A T E C H A N G E I N F L U E N C E O N S O I L F O O D W E B 2113
prompted calls for an integration of disciplinary knowledge (Van Der Putten et al., 2004; Shennan, 2008).
Plants directly or indirectly control and mediate all
soil multitrophic interactions. Root exudates, sloughed
off root tissue and rhizodeposition attract bacteria, fungi
and nematodes as pathogens or parasites of live roots.
As plants die, canopy and root litter continue to supply
nutrients to these and other microbes operating as saprophytes and other functional groups. Plants determine
the composition of fungal and bacterial communities in
the rhizosphere through the production of specific
flavonoids in root exudates (Straney et al., 2002). Other
specific chemical signals control associations between
plant roots and mycorrhizae (Shefferson et al., 2007),
and pathogens and plant growth promoting organisms
(Haas & Defago, 2005). Glucosinolate produced by
cruciferous plants decomposes in soil into compounds
that act as a fumigant against soil-borne pathogens
(Gimsing & Kirkegaard, 2009) and other microbes such
as nitrifying bacteria (Brown & Morra, 2009).
The role of overall biodiversity in soil multitrophic
interactions is not well understood. This is unlike in terrestrial multitrophic interactions where a loss of biodiversity affects the delivery of ecosystem services
(Hooper et al., 2005; Cardinale et al., 2006; Scherber
et al., 2010). This poor understanding is largely because
only 0.1% of soil fungi and bacteria have been cultured
and assigned clear metabolic roles (Barrios, 2007). The
difficulty of linking biodiversity to function persists
despite the use of metagenomics (Elsas et al., 2008) and
other molecular tools to expand our knowledge of biodiversity (Beed et al., 2011) and the functional potential
of species or communities (Phillips et al., 2003; MonteroBarrientos et al., 2010). Although increased activity of
more diverse soil food web points to the importance of
biodiversity in soil multitrophic interactions (Krumins
et al., 2006), the effect of species richness decreases with
trophic distance (Scherber et al., 2010) and biodiversity
may have a different role at each trophic level.
There is some evidence that microbial diversity per se
is not necessary at least for soil carbon sequestration
(King, 2011). Carbon is sequestered in soil aggregates
(Blanco-Canqui & Lal, 2004) and Arbuscular mycorrhizae (AM) (Bedini et al., 2009), saprophytic fungi and
bacteria contribute to the formation and stabilization of
soil aggregates (Gupta, 2011). Differences in community composition do not explain differences in organic
matter content of soils (Kim et al., 2007).
In this review we recognise two distinct spatial and
functional domains under ‘stress tolerance’ and ‘pathogen suppression’ as components of soil food web
(Fig. 1) to help improve understanding of the constituent multitrophic interactions and to reinforce the primacy of plants as the driver of multitrophic interactions
© 2012 Blackwell Publishing Ltd, Global Change Biology, 18, 2111–2125
(Scherber et al., 2010; Johnson et al., 2011). Multitrophic
interactions involved in pathogen suppression operate
in the rhizosphere where bacteria, fungi, nematodes,
protozoa and possibly other microbes perform specific
functions to help suppress infection and colonisation of
plant roots by pathogenic microbes. Multitrophic interactions that impart stress tolerance to plants also operate in the rhizosphere and involve mycorrhizae,
endophytic fungi, bacteria and viruses. This distinction
is not to detract from the important role of soil food web
or its network of multitrophic interactions but to propose a framework to help synthesise cross-disciplinary
knowledge. All trophic processes including parasitism,
predation, competition and mutualism are essential elements of the overall soil food web (Susilo et al., 2004;
Lambers et al., 2009), but only specific combinations of
microbes and trophic processes deliver stress tolerance
or pathogen suppression. Also, the same group of
organisms can participate in different multitrophic
interaction networks. Necrotrophic fungi, for instance,
use enzymes and other chemicals to decompose organic
matter but use a very different set of virulence factors to
invade living plant tissue as a pathogen.
Soil food web
Soil food web is the network for the transfer of energy
among and between communities of organisms living
all or part of their lives in the soil ecosystem (Barrios,
2007; Blankinship & Hungate, 2007). In its simplest
form, soil food web shows ‘connectivity’ between various species, groups or feeders; while food webs showing the ‘transfer of energy’ between organisms at
various trophic levels are at the next level of complexity; and webs showing per capita ‘interaction strengths’
between organisms are among the most detailed to
offer functional insights. However, there is a lack of
integration of horizontal and vertical complexity and
biodiversity within and between trophic levels, respectively, and their interactions (Duffy et al., 2007). Consequently, knowledge of soil food web is fragmented.
Models incorporating elements of belowground interactions suffer from deficiencies and are not often validated using independent data (Matthews et al., 2004).
Energy flows from primary producers to higher trophic levels via one of three basic channels, (a) bacterial
channel of saprophytic and pathogenic bacteria and
their consumers; (b) fungal channel of saprophytic,
mycorrhizal and pathogenic fungi; and (c) the root
energy channel of herbivores, nematodes, bacteria,
micro-arthropods and their consumers (Moore et al.,
1988; Holtkamp et al., 2008). However, food webs are
dynamic energy flow systems without a fixed structure
over time and both bacterial and fungal energy channels
2114 S . C H A K R A B O R T Y et al.
Climate and atmospheric composiƟon
MulƟtrophic interacƟonmediated feedback to
global climate
Plant-mediated
influence of climate
change
Above-below
ground interacƟons
LiƩer
Root feeding
Protozoa
Endophyte
mutualism
Grazing resistance
DETRITOSPHERE
Nematode
predaƟon
ISR elicitaƟon
Bacteria
Growth promoƟon
AnƟbiosis
compeƟƟon
symbiosis
Mycorrhiza
RHIZOSPHERE
Stress tolerance
DecomposiƟon
Fungi
Pathogen suppression
Arthropods
Grazing
MineralisaƟon
pathogenicity
Soil food web
DRILOSPHERE
Earthworms
Fig. 1 A conceptual diagram of plant-mediated influences of climate change on soil food web and feedback to global climate showing
important niches (in capital), and processes and mechanisms (in italics) involved in the network of multitrophic interactions between
plants as the primary producer and soil organisms in the overall soil food web and its two constituent multitrophic interactions
involved in pathogen suppression and stress tolerance (delineated by dotted line). Arrows with solid lines represent known interactions and arrows with dashed lines represent processes and interactions that are not clearly understood.
operate simultaneously in most soil food webs with
temporal and spatial variation (Hassall et al., 2006). The
dominance of fungal or bacterial energy channels are
often determined by the quality and quantity of
soil organic matter (Holtkamp et al., 2008). Soil food
webs with bottom-up trophic control where biomass
and energy transfers from lower to higher trophic
levels (Scherber et al., 2010) are influenced by nutrient
availability.
Multitrophic interactions involved in pathogen
suppression
Soil-borne pathogens are responsible for 90% of diseases that affect major crops in the USA (Lewis &
Papavizas, 1991) and together with parasitic nematodes
inflict enormous loss to agriculture each year (Lumsden
et al., 1995; Bird & Kaloshian, 2003). Fungal pathogens
in soil are necrotrophs that derive nutrition from dead
organic substrates but have the capacity to infect and
kill live plant roots by producing toxins and other substances. Their broad host range and saprophytic ability
allows them to sustain large populations.
Plant pathogens are important in the structure and
function of food webs (Borer et al., 2007; Holdo et al.,
2009; Olofsson et al., 2011), but their importance
extends beyond food webs. At the ecosystem level,
pathogens influence the structure, composition and
evolution of plant communities (Dobson & Crawley,
1994; Roy et al., 2004; Kardol et al., 2006) affecting the
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delivery of ecosystem services (Cheatham et al., 2009)
including carbon exchange (Olofsson et al., 2011). The
soil borne pathogen Phytophthora cinnamomi has altered
some Australian forest communities by replacing susceptible Eucalyptus trees with resistant sedge and grass
communities while another soil borne pathogen, Phellinus
weirii, has been a major agent for forest disturbance in
North America (Alexander, 2010).
Soil health and pathogen suppressiveness are two
important aspects that function due to multi-species
interactions between organisms at different trophic levels (Verhage et al., 2010), but their multitrophic nature
has not always been explicitly demonstrated. Soil quality and soil health are related concepts used to designate the functional and/or productive status of soil.
There is considerable scientific debate about the concepts and indicators to measure soil quality and health
(Van Bruggen & Semenov, 2000; Janvier et al., 2007).
Using keystone species like Rhizobium, or soil dwelling
nematodes and their trophic groups provide workable
estimates of soil health, but methods that combine
physical, chemical and biological parameters, make
them cumbersome and expensive (Van Bruggen &
Semenov, 2000; Pattison et al., 2008).
Suppressive soils are ‘soils in which disease severity
or incidence remains low, in spite of the presence of a
pathogen, a susceptible host, and climatic conditions
suitable for disease development’ (Baker & Cook, 1974).
Soils suppressive to fungal and bacterial pathogens and
nematodes have been described. Different mechanisms
have been postulated to explain suppressiveness
including microbial diversity and composition, population size of certain groups or species, competition
for nutrients, antibiosis and predation by amoebae
(Chakraborty et al., 1983).
Pseudomonas, Lysobacter and other bacteria and nonpathogenic Fusarium and Trichoderma species are implicated in the suppression of fungal pathogens including
Gaeumannomyces graminis var. tritici, Pythium ultimum
and Thielaviopsis basicola (Haas & Defago, 2005; Borneman & Becker, 2007; Postma et al., 2010). Antibiosis,
induced systemic resistance (ISR) and specific pathogen-antagonist interactions are three modes of action
involved in pathogen suppression by bacteria (Haas &
Defago, 2005). Strains of the fungus, Trichoderma harzianum commonly found among rhizosphere organisms
also trigger ISR (Shoresh et al., 2010). ISR makes plants
more resistant to necrotrophic fungal pathogens, some
viruses and insects, and it extends to all parts of a plant.
Some Actinobacteria form endophytic relationships
to protect roots from infection by several fungal pathogens (Franco et al., 2007).
The protection of host roots by ISR and antibiotic production also promotes plant emergence and growth.
© 2012 Blackwell Publishing Ltd, Global Change Biology, 18, 2111–2125
These changes in plant composition and signalling
pathways link soil microbe – plant interactions to
aboveground trophic processes such as herbivory
(Pineda et al., 2010). Other changes such as pathogeninduced mycotoxin in cereals makes straw attractive to
earthworms and leads to its rapid decomposition
(Wolfarth et al., 2011).
Multitrophic interactions involved in stress tolerance
Mutualism by mycorrhizae and endophytes confers
benefits such as nutrient acquisition and stress tolerance to their plant hosts (Frey-Klett et al., 2007). Mycorrhizae mediate plant nutrient foraging, carbon
allocation and root architecture, changes in soil structure and soil carbon storage (Staddon et al., 2002), and
shift plant communities by suppressing non-mycorrhizal
species (Cameron, 2010; Klironomos et al., 2011).
Ectomycorrhizal fungi (EM) proliferate outside the root
and form a sheath around the root as a physical barrier
to protect against pathogens by antibiosis and by inducing fungistatic compounds (Duchesne, 1994). AM form
arbuscules as sites of energy transfer between the host
and fungus, and vesicles or hyphal swellings as storage
organs (Rillig, 2007). AM enhance nutrient uptake by
the plant, prevent root infection by pathogens and stimulate plant defence by lignification (Azcón-Aguilar &
Barea, 1997). AM increase host plant fitness by modulating multitrophic interactions (Hoffmann et al., 2011).
An example of multitrophic interactions involving AM
and EM is their association with members of Pseudomonas, Bacillus, Klebsiella and Streptomyces as mycorrhiza
helper bacteria (Frey-Klett et al., 2007). This association
makes the mycorrhizal symbiont more effective in
mobilising soil nutrients, fixation of atmospheric
nitrogen and the protection of roots against soil borne
pathogens.
Endophytic fungi reside entirely within plant tissues
and emerge to sporulate at plant senescence (Bacon
et al., 1991). This association, ranging from mutualistic
to parasitic, can confer tolerance to environmental
stress such as heat and water stress (Rodriguez et al.,
2009). Endophytes enhance survival and primary production of host plants (Newsham, 2011), prompting
suggestions for their use for climate change mitigation
(Redman et al., 2011).
Many endophytes produce alkaloids and other secondary fungal metabolites that offer resistance to
intense grazing from animals, insect herbivores and
pathogens (Pineda et al., 2010). A typical example of
multitrophic interaction involving an endophyte is the
symbiosis between a virus-infected Curvularia protuberata and its grass host Dichanthelium lanuginosum
(Márquez et al., 2007). Neither the fungus nor its host
2116 S . C H A K R A B O R T Y et al.
plant can grow in geothermal soils above 38 °C, but
when the fungus is infected by a virus, the plant can
grow at soil temperatures of 50 °C. This thermotolerance allows the plant to thrive in soils where annual
temperatures fluctuate between 20 and 50 °C.
Climate change influence on soil multitrophic
interactions
Recent reviews have dealt with climate change influence on some aspects of soil food web such as, beneficial and harmful organisms (Compant et al., 2010;
Pritchard, 2011), genetic resources of soil micro-organisms (Beed et al., 2011), soil community response to
warming and precipitation (Briones et al., 2009; Hawkes et al., 2011), rhizosphere microbial community
response to rising atmospheric CO2 (Drigo et al., 2008),
and climate change influence on mycorrhizae (Nannipieri,
2011) and plant pathogens (Chakraborty & Newton,
2011). With only a single review dealing with soil food
web (Blankinship & Hungate, 2007), a comprehensive
analysis of climate change impact on soil multitrophic
interactions has been lacking.
Influences will be mediated through qualitative changes
in plant
Climate change influence on soil organisms and their
multitrophic interactions will be mostly plant mediated
(Johnson et al., 2011). Qualitative changes in physiology, tissue composition and signalling pathways under
rising CO2 may influence soil multitrophic interactions.
As CO2 levels in soil pores often exceed projected
future atmospheric concentrations by several fold
(Flechard et al., 2007), CO2 may not directly influence
multitrophic interactions. Plants with increased root
growth and root to shoot ratio at elevated CO2 will
modify root architecture, exudation of labile compounds in the rhizosphere and root turnover rate
(Pritchard, 2011) to influence plant-pathogen and plantmycorrhiza interactions (Melloy et al., 2010; Eastburn
et al., 2011; Pickles et al., 2012). Unlike CO2, warming
will directly influence multitrophic interactions if rises
in soil temperature exceed the buffering capacity of
soils. Indirect influences of temperature will be mediated through changes in the quality, quantity, species
composition and structure of plant communities.
Of particular interest are the large number of plant
genes and gene networks and some hormones that are
regulated in a coordinated manner in response to infection by fungal pathogens, cold or drought stress (Singh
et al., 2002; Eastburn et al., 2011) and insect herbivory
(Verhage et al., 2010), albeit with different signalling
pathways (Ramı́rez et al., 2009). Table 1 lists some
examples of changes to the structure, composition and
signalling pathways of plants under climate change
and their influence on plant-microbe interactions from
a multitrophic interactions perspective. This list is neither exhaustive nor definitive, as plants can respond in
a different way to heat and drought stress when
applied together compared with each stress being
applied separately (Rizhsky et al., 2002). A comprehensive list of host-pathogen changes in response to elevated CO2 and O3 has recently been published
(Eastburn et al., 2011).
Root maintenance respiration increases with rising
soil temperature, increasing root turnover and reducing
root longevity (Pritchard, 2011). Root production and
turnover increases with raised soil water content, leading to increased root surface area for microbial colonization and herbivory (Gill & Jackson, 2000). The
composition, diversity and productivity of plant communities change with changing precipitation pattern to
influence belowground interactions (Suttle et al., 2007)
including those involving mycorrhizae and pathogens.
Geographical distribution of plants will change with
changing temperature and precipitation. One estimate
projects a 51% reduction in the 32 million hectares of
highly productive area under wheat, covering northwestern Mexico, the Indo-Gangetic plains and the Nile
valley (Ortiz et al., 2008). Changed distribution will
cause habitat fragmentation and expose plant communities to new stresses if soils and other conditions are
unsuitable in areas with suitable climate. The poleward shift of plant species and changes in species
assemblages due to warming of about 3 °C can be more
important for soil organisms than the direct effects of
warming (Wardle, 2002). At least in the short-term
there will be an uncoupling of above and belowground
multitrophic interactions, and new networks may
evolve (Van Der Putten et al., 2010).
Climate change influence on soil food web
Increased abundance and altered quality of plant litter
at elevated CO2 will influence microbial decomposition
of litter and the release of nutrients. In general,
decreased nitrogen concentration and increased carbohydrate and phenolics increase the carbon/nitrogen
ratio of plant litter at high CO2. While some studies
show a delayed degradation of plant litter produced at
high CO2 (Ulainen et al., 2003), a meta-analysis failed to
show any overall delay in litter degradation (Norby
et al., 2001). However, as most studies have used soil
respiration as an indicator of microbial activity, the
influence of altered litter quality on the structure and
function of soil communities and their subsequent
influence on soil food web remains unclear. Herbivores
© 2012 Blackwell Publishing Ltd, Global Change Biology, 18, 2111–2125
Element of
climate change
Drought
Drought
Drought
Elevated CO2
Elevated CO2
Elevated CO2
Elevated CO2
Elevated CO2
Elevated CO2
Elevated CO2
Plant
Arabidopsis thaliana
Arabidopsis thaliana
Hordeum vulgare
and others
Brassicaceae family
Acer rubrum
© 2012 Blackwell Publishing Ltd, Global Change Biology, 18, 2111–2125
Nicotiana tabacum
Glycine max
Solidago rigida
Hordium vulgare
Several species
↑Glucosinolate
↓Stomatal conductance
↑Phenolics & tannins
↑Plant defence against pathogen
↓Leaf nicotine
↑Phytoalexin Glyceollin in resistant plants
↑Plant defence against pathogen
↓Nitrogen concentration
↑Net photosynthesis
↑Papillae production
↑Silicon accumulation
↓Nitrogen concentration
↑Phenolics
Induced resistance to pathogens
↑Abscisic acid
↑Stomatal closure
↑Abscisic acid
↑Methyl jasmonate
↓Shoot and root biomass
↑Shoot N
Potentially delayed litter degradation
Increased resistance to potato virus Y
Potentially increased resistance to fungal pathogen
Phytophthora sojae from ß-glucan elicitor
Reduced fungal leaf spot by Cercospora and Septoria
Reduced fungal penetration by Blumeria graminis
Reduced disease incidence by fungal pathogen
Botrytis cinerea
Reduced effect of drought by earthworm Aporrectodea
caliginosa
Reduced aphid abundance
Increased number of parasitoid
Reduced soil microbial population
Reduced foliar disease incidence by fungal pathogen
Phyllosticta minima
Influence relating to multitrophic interactions
Change(s) in plant response
(Lindroth, 2010)
(Strengbom & Reich, 2006)
(Hibberd et al., 1996)
(Matros et al., 2006)
(Braga et al., 2006)
(Schonhof et al., 2007)
(McElrone et al., 2005)
(Johnson et al., 2011)
(Ramı́rez et al., 2009)
(Jakab et al., 2005)
Reference
Table 1 Selected examples of changes in plant form and function under elements of climate change with demonstrated/potential effect on microorganisms involved in multitrophic interactions in soil, with arrows indicating an increase (↑) or decrease (↓) in plant response
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2118 S . C H A K R A B O R T Y et al.
and soil invertebrates feeding on plant tissue containing high levels of secondary or structural compounds
show reduced growth, development and population
densities, with potential impacts on soil food web
(Lindroth, 2010). Herbivory also increases due to compensatory feeding on plant tissue with reduced nutritional value (Schadler et al., 2007).
A high carbon/nitrogen ratio of plant litter and the
exudation of organic carbon compounds may shift soil
food webs from bacteria to fungi-dominated (Drigo
et al., 2007), increasing fungal abundance across different ecosystems (Janus et al., 2005; Lipson et al., 2006).
Mycorrhiza and heterotrophic fungi may also be
boosted by increased photosynthesis and transfer of
carbon to fine roots (Bardgett et al., 2008), but this will
be moderated by shifts in the composition and diversity
of the vegetation. Some plants may selectively enrich
certain fungi by secreting toxins in soil (Van Der
Putten, 2009).
Findings on bacteria are variable. Some CO2-enrichment studies show a stimulation of rhizosphere bacteria including nitrogen-fixing rhizobia and increased
size and number of root nodules (Compant et al., 2010;
Pritchard, 2011) and increased bacterial biomass (Drigo
et al., 2008), while others show no general trend (Zak
et al., 2000).
Elevated CO2 can boost population size, colonisation,
and/or diversity of AM and EM fungi (Compant et al.,
2010). A meta-analysis of 65 field studies where mycorrhizal response to CO2 enrichment was measured for
> 2 months, showed a 47% increase in growth of AM
or EM (Treseder, 2004). AM association supplies all of
the plant phosphorous nutrition in some crops (Smith
et al., 2004). The boost in AM population could further
improve the acquisition of phosphorous, nitrogen,
zinc and other nutrients (Cavagnaro et al., 2011). But
the benefit to mycorrhizal association from CO2 enrichment will be determined by phosphorous and nitrogen
availability in soil.
At the second trophic level there is no significant and
consistent response of high CO2 in the majority of over
50 studies (Blankinship & Hungate, 2007). At the third
trophic level, population size and/or diversity of some
root feeding nematodes (Yeates & Newton, 2009) and
collembolans increase with CO2-enrichment. But other
studies show no change (Hungate et al., 2000), or
enrichment of nematodes only under low fertility (Li
et al., 2009), pointing to the complexity of these interactions. Eight out of 15 studies of the third trophic level
showed increased abundance or activity, six showed no
change and one showed a reduction of bacterivores
and/or fungivores but individual groups such as protozoa, enchytraeid and nematodes did not show any consistent trend (Blankinship & Hungate, 2007). In one
long-term study, the effect of elevated CO2 on fungal
communities was transmitted to higher trophic levels
and influenced the abundance and species composition
of fungal feeders (Jones et al., 1998). Nevertheless, the
relationships between community structure and CO2
enrichment are complicated by spatial heterogeneity
and other factors (Ge et al., 2010).
Soil microbial activity and mineralization are
increased in warmer soils (Gill & Jackson, 2000) before
acclimation reduces temperature sensitivity (Balser
et al., 2006), but changes in litter quality and physiology
of soil organisms at high temperatures modify these
(Heinemeyer et al., 2006). Fungal populations and nematodes grazing on fungi and bacteria generally increase
due to warming, while nematode diversity is reduced
despite increased growth, fertility and mobility (Convey & Wynn-Williams, 2002; Blankinship & Hungate,
2007). Soil water content can modify the effect of rising
temperatures. The algal-feeding Endorylaimus that prefers a moist habitat, increases under warming in preference to microbe-feeding nematodes (Simmons et al.,
2009). Increasing soil temperature generally decreases
soil microbial biomass in controlled experiments
but long term field studies either show no effect or a
positive effect (Pritchard, 2011).
Decreased precipitation and repeated wetting of soils
reduce both bacterial and fungal biomass but fungal
dominated food webs respond more readily to changing precipitation (Hawkes et al., 2011). Altered precipitation regulates the population of microbial grazers and
bacterial-feeding nematodes are more sensitive to
drought than fungal feeders (Landesman et al., 2011).
Drier conditions can lead to changes at higher trophic
levels due to bottom-up resource limitation as soil
organisms appear to be more sensitive to dry conditions than to increased precipitation. Increased precipitation generally benefits detritivores and herbivores at
the second trophic level.
Climate change influence on multitrophic interactions
involved in pathogen suppression
Increased concentration of plant phenolics (Hartley
et al., 2000; Percy et al., 2002) and tannins (McElrone
et al., 2005) at high CO2 directly increases the resistance
of plant tissue to pathogen invasion. Phenolics are antifungal compounds with a well-established role in
defence against pathogens and herbivores, and flavonoids are involved in plant-pathogen signalling (Bednarek & Schulze-Lefert, 2009). These and other changes
in host plants at high CO2 may affect survival, ecological/reproductive fitness and/or the severity of diseases
caused by soil borne pathogens. Increased photosynthesis and water use efficiency raise tolerance of tomato
© 2012 Blackwell Publishing Ltd, Global Change Biology, 18, 2111–2125
C L I M A T E C H A N G E I N F L U E N C E O N S O I L F O O D W E B 2119
roots to Phytophthora parasitica infection (Jwa & Walling,
2001); increased b-1, 3 glucanase reduce potato leaf
necrosis due to Phytophthora infestans (Plessl et al.,
2007); and production of the phytoalexin glyceollin
increases resistance in soybean in response to an elicitor
from Phytophthora sojae (Braga et al., 2006). The concentration of Glucosinolate can increase under elevated
CO2 (Schonhof et al., 2007), but how this increase
impacts on pathogens, other soil microbes and their
multitrophic interactions has not been addressed.
Altered rhizodeposition and root exudates under elevated CO2 boost the frequency of iron-chelating Pseudomonas spp. (Tarnawski et al., 2006) and rhizosphere
populations of other microbes associated with pathogen suppression. These and other rhizosphere bacteria,
collectively known as plant growth promoting bacteria,
stimulate plant growth by producing growth-promoting hormones, alleviating biotic and abiotic stresses
and imparting ISR to plants (Hardoim et al., 2011). Populations of some plant growth promoting bacteria such
as Pseudomonas and Actinobacteria are selectively
enriched by certain host plants under CO2 enrichment
(Compant et al., 2010). Nevertheless, the overall impact
on pathogen suppression is difficult to predict due to a
lack of understanding of important interacting factors.
For instance, the biomass of Fusarium pseudograminearum increases per unit of plant tissue at high CO2
increasing the amount of inoculum (Melloy et al., 2010).
Potentially this may balance the effects of increased
populations of suppressive microbes. But this cereal
pathogen has low saprophytic fitness and can be rapidly eliminated from organic matter by other microbes
including fungi (Pereyra et al., 2004) and nematodes
(Wolfarth et al., 2011).
The resistance to Fusarium subglutinans increases in
pineapple under raised temperatures (Matos et al.,
2000), but the influence is species-specific (Chakraborty
& Newton, 2011; Eastburn et al., 2011). High temperature reduces resistance against Phytophthora infestans in
potato (Mizubuti & Fry, 1998), against Fusarium oxysporum
f. sp. ciceris in chickpea (Landa et al., 2006) and against
two bacterial pathogens in pepper, but resistance
remains unchanged against two fungal pathogens in
pepper (Shin & Yun, 2010).
Crop plants now grow in areas where soil and climate are very different to their centres of origin. Often
pathogens have migrated with their host, expanding
their range. This trend is likely to continue with rising
temperature as cropping areas shift pole-ward. Warming will expand the geographical range of Phytophthora
cinnamomi (Bergot et al., 2004; Desprez-Loustau et al.,
2007); increase the risk of severe Phytophthora infestans
epidemics (Hannukkala et al., 2007) and the number of
Meloidogyne incognita generations (Ghini et al., 2008). At
© 2012 Blackwell Publishing Ltd, Global Change Biology, 18, 2111–2125
least in the short term, habitat fragmentation is likely to
uncouple above and belowground multitrophic interactions, which control the biological suppression of soil
borne pathogens.
The literature on the effect of drought (McElrone
et al., 2003; Cotty & Jaime-Garcia, 2007), flooding (Barta
& Schmitthenner, 1986) and rainfall (Bowers et al.,
1990) on plant pathogens show species-specific
responses. A meta-analysis indicates that insect and
pathogen feeding behaviour, plant parts affected and
the severity of water stress are important factors that
determine the impacts of changing precipitation on
pathogens (Jactel et al., 2012).
Realistic impact assessment requires the combined
influence of changing temperature, soil moisture and
CO2 on pathogen suppressiveness. As pasteurisation
removes some forms of soil suppressiveness, pathogen
suppression may be eliminated by small rises in soil
temperature (Borneman & Becker, 2007; Bent et al.,
2008). Under experimental conditions, Gaeumannomyces
graminis var. tritici, survives in cool dry soils but a
moist soil > 30 °C eliminates the pathogen within
3 months (Wong, 1984). However, these findings may
not apply directly to field soils which are buffered from
the effect of rising temperatures. Suppression of the
potato common scab pathogen in cold and wet soil by
volatile secondary metabolic gases from Pseudomonas,
Bacillus and Streptomyces becomes ineffective in hot and
dry soils (Sturz et al., 2004). Other interactions in the
rhizosphere will be favoured under rising temperatures. Strains of plant growth promoting bacteria
including rhizobia that grow better at high temperature
will dominate under warming to alleviate temperature
and drought stress (Compant et al., 2010). Plants such
as sunflower growing under drought stress may select
strains of Achromobacter that offer higher growth
promotion under drought (Forchetti et al., 2007).
Climate change influence on multitrophic interactions
involved in plant stress tolerance
Elevated CO2 can boost populations of mycorrhizal
fungi and selectively enrich species or strains efficient
at acquiring mineral nutrients (Pritchard, 2011).
Increased levels of plant phenolics at high CO2 boost
mycorrhizal spore germination and colonisation, and
certain flavonoids boost hyphal branching in AM
(Scervino et al., 2007). This may increase nutrient and
water uptake, overall fitness and health of plants to
potentially increase their stress tolerance. However,
these benefits will depend on the dynamics of fine root
turnover rate, and the equilibrium between soil mineral
nutrients and carbon fixation by plants (Pritchard,
2011).
2120 S . C H A K R A B O R T Y et al.
Colonisation by some endophytic fungi can increase
at elevated CO2 leading to changes in biomass and
chemical composition of plants, including alkaloid,
protein and carbohydrate levels (Newsham, 2011).
Elevated CO2 increased colonisation of Lolium arundinaceum by Neotyphodium coenophialum but decreased concentrations of ergovaline and loline alkaloids (Brosi
et al., 2011). However, endophytes have failed to
improve plant function at elevated CO2 in some studies
(Alberton et al., 2010).
Warming generally increases root colonization and
hyphal length by AM but findings are varied on EM
from limited studies (Compant et al., 2010). Warming
increases mycorrhizal colonization by directly stimulating fungal growth and indirectly by stimulating plant
growth to accelerate the rate of transfer of plant photosynthates to the symbiont (Hawkes et al., 2008). Mycorrhizal response to warming is modulated by the
duration of warming (Simard & Austin, 2010), and the
acclimatization of the symbiont community over time
(Deslippe et al., 2011). Warming alters the structure of
mycorrhizal networks (Hawkes et al., 2008; Deslippe
et al., 2011). Larger EM networks under warming may
explain the expansion and dominance of Betula nana in
the Arctic plant community (Clemmensen et al., 2006).
Drought generally reduces mycorrhizal colonisation
but the response is species-specific and EM may be
more severely affected than AM. This can influence the
competition between AM-shrubs and EM-trees. Mycorrhizae can make its host drought tolerant by improving
water uptake by roots, tolerance of lower xylem pressure, greater lateral root formation, and osmotic adjustment to avoid dehydration (Compant et al., 2010).
Warming generally favours endophytic colonisation
that protects the host plant from abiotic stress. The
influence of elevated CO2, warming and precipitation
on Lolium arundinaceum–Neotyphodium coenophialum
interaction has revealed complex but interesting findings (Brosi et al., 2011). Contrary to previous studies,
endophytic colonisation was not affected by warming
or precipitation. Warming increased loline concentrations by 28% but had no effect on ergovaline. The two
alkaloids influence two different groups of grazers with
very different ecological and economic significance.
Consumption of ergovaline containing plant materials
causes ‘tall fescue toxicosis’ in livestock, with symptoms of poor weight gain, reduced fertility and lactation, and gangrene (Panaccione et al., 2001). Loline
alkaloids, on the other hand, have insecticidal properties making their host plant tolerant to insect and nematode attack (Yule et al., 2011). By enhancing the
insecticidal property of tall fescue pastures without
increasing their detrimental effect on livestock grazing,
climate change may have an overall beneficial effect.
Conclusions and recommendations
Summarising the influence of climate change on soil
multitrophic interactions is a daunting task due to an
overall paucity of knowledge and a lack of clarity on
the ecological networks that constitute these interactions. The scant literature is fragmented along disciplinary lines, often reporting inconsistent findings that are
context and scale-dependent. We have argued for the
differentiation of soil multitrophic interactions along
functional and spatial domains as a framework to synthesise cross-disciplinary knowledge. Distinct from litter mediated interactions in detritosphere or elsewhere
in the soil, the proposed ‘pathogen suppression’ and
‘stress tolerance’ interactions operate in the rhizosphere. While partitioning soil multitrophic interactions
into functional domains will improve understanding,
these networks must be mechanistically linked to reproduce all functionalities of the overall soil food web.
A review of the literature suggests that climate
change will influence the relative importance, frequency
and composition of functional groups, their trophic
interactions and processes controlling these interactions. The key influences of elevated CO2 and temperature, and changed precipitation are summarised for the
three networks of multitrophic interactions (Table 2).
Soil microbial resources offer great promise in
improving tolerance of plants to biotic and abiotic stresses (Mazzola, 2010; Pritchard, 2011), but amendments
to enhance nutrient availability, disease suppressiveness or biological control of pests and pathogens often
give inconsistent results (Juroszek & Von Tiedemann,
2011). Climate change will increase uncertainty by giving rise to novel interactions and by uncoupling above
and belowground multitrophic interactions (Van Der
Putten, 2009). Even without climate change considerations, improved understanding of soil multitrophic
interactions will have definite scientific and practical
benefits in managing soil biota.
Improved understanding of soil multitrophic interactions is a prerequisite to predicting how a changing climate will influence these interactions to impact on the
delivery of vital ecosystem services. A lack of clarity on
soil multitrophic interactions has obscured important
processes such as the sequestration of carbon in soil
and its release from organic matter and feedback to global climate systems despite much research. There is a
risk of multiplying ignorance without a clear framework and well-formulated research questions. We
propose four major lines of enquiry.
Improved understanding of soil multitrophic interactions
Additional baseline information on specific soil multitrophic interactions has to be the foundation for any
© 2012 Blackwell Publishing Ltd, Global Change Biology, 18, 2111–2125
C L I M A T E C H A N G E I N F L U E N C E O N S O I L F O O D W E B 2121
Table 2 A summary of observed and potential influence of climate change on soil multitrophic interactions (MI)
Soil MI
Elevated CO2
Elevated temperature and changed precipitation
Soil food
web
Increased litter and roots with altered quality
Potentially delay litter decomposition and nutrient
cycling
Potential fungal domination of soil food web
Stimulation of N2-fixing bacteria
Inconsistent findings on multitrophic interactions
Increased fungal and nematode population
Increased mineralisation
Fungi dominated food webs respond more
readily to moisture changes
Drier conditions influence trophic interactions
due to bottom-up resource limitation
Pathogen
suppression
Increased resistance to fungal pathogens due to rising
secondary metabolites
Growth stimulation and changed mycorrhizal
community
Improved plant health from increased activity of plant
growth promoting bacteria
Pathogen suppression determined by the balance
between increased pathogen inoculum and population
of suppressive microbes
Enhanced mycorrhizal growth
Pole-ward shift of plants and their pathogens
from changed climate suitability
Necrotrophic pathogens becoming more
damaging if plants are stressed in the new
environment
Uncoupling of above and below ground links
due to habitat fragmentation
Altered effectiveness of disease resistance genes
Plant stress
tolerance
Boosted population and diversity of mycorrhizae and
enrichment of species efficient at nutrient acquisition
Boosted phosphorous and nitrogen nutrition of plants
Increased stress tolerance and plant defence against
herbivore and pathogen
Potentially improved stress tolerance from increased
alkaloid production by endophytes
Improved stress tolerance from increased
mycorrhizal colonisation
Potentially increased biotic and abiotic stress
tolerance in combination with high CO2
improved understanding. Empirical and modelling
approaches will be equally important in balancing roles
and links between the functional domains and multitrophic interaction networks. The lack of understanding
of soil multitrophic interaction multiplies with increasing
spatial and temporal scales. One approach will be to use
a combination of process and organism-oriented models
with the flexibility to incorporate new properties that
become evident only at a higher spatial/trophic level.
Linking biodiversity to function
The use of molecular tools has greatly expanded knowledge of soil microbial biodiversity but its role in multitrophic interactions is yet to be addressed. A large
biodiversity by itself is not enough for soil resilience.
The functional potential of soil biota has to be optimally
expressed under climate change and determining thresholds
for important interactions between functional groups
will be essential. Other characteristics that determine
soil resilience and sustainability, and how these are
influenced by climate change will be important to understand the buffering and inherent adaptive capacity of soils.
Influence of combinations of climatic factors on
multitrophic interactions
Most studies have mainly dealt with the influence of
single climatic factors such as elevated temperature
© 2012 Blackwell Publishing Ltd, Global Change Biology, 18, 2111–2125
and/or CO2 on specific interactions at lower trophic
levels over short to medium time periods. A multi-factorial approach (Singh et al., 2010) based on realistic
field studies using temperature and CO2 gradients to
mimic gradual climate change (Chakraborty et al.,
2008) will avoid overestimation of community response
to abrupt rise in CO2 (Klironomos et al., 2005). These
studies are necessary to identify processes that will be
significantly altered and to develop options to maintain
ecosystem services. New research must also address
how multitrophic interactions will cope with increased
frequency and magnitude of extreme events.
Evolutionary ecology of multitrophic interactions in a
changing climate
Soil microbial communities can rapidly adapt to elevated CO2 (Allison et al., 2010), temperature (Compant
et al., 2010) and raised fecundity at high CO2 can accelerate micro-evolution (Chakraborty & Datta, 2003). But
evolutionary ecology is not often considered for soil
organisms (Hassall et al., 2006). Multitrophic interactions are an important driver of selection processes for
organisms and functional groups to alter their ability to
adapt to a changing climate, and/or new geographical
range (Van Der Putten et al., 2010). New long-term
research on climate change mediated evolution of microbial communities and their multitrophic interactions,
with or without habitat fragmentation, will be essential.
2122 S . C H A K R A B O R T Y et al.
Acknowledgements
This review stems from an invited presentation by the senior
author at the 6th IOBC working group meeting on multitrophic
interactions in soil held in Cordoba, Spain during 4–7 April
2011. We acknowledge the numerous discussions with colleagues in forming opinions expressed in this review. Some of
the findings come from research by graduate students including
Peter Wilson, Femi Akinsanmi, Rhyannyn Westecott and Paul
Melloy and technical assistance from Ross Perrott. Co-investment in research from the Cooperative Research Centre for
National Plant Biosecurity, CSIRO Plant Industry and the
Grains Research and Development Corporation is gratefully
acknowledged.
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