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Mycorrhizas as nutrient and energy pumps of soil food webs: multitrophic interactions and feedbacks



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Mycorrhizal Mediation of Soil © 2017 Elsevier Inc. All rights reserved.
Mycorrhizas as Nutrient
and Energy Pumps of Soil Food
Webs: Multitrophic Interactions
and Feedbacks
P.M. Antunes, A. Koyama
Algoma University, Sault Ste. Marie, ON, Canada
Mycorrhizal fungi form bridges among the rhizospheres of different plants through which
organic carbon (C), nutrients [e.g., nitrogen (N) and phosphorus (P)], allelochemicals, bac-
teria, and viruses can travel either inside the hyphae or attached to the hyphosphere. Plant
roots can be a quantitatively more important source of C for soil food webs than above-
ground litter in temperate forests (Pollierer et al., 2009, 2012) and agroecosystems (Kramer
et al., 2012), and mycorrhizal networks represent an important channel for this C. In this
chapter we will review how the most abundant types of mycorrhizal fungi [i.e., ectomycor-
rhizal (EcM) and arbuscular mycorrhizal (AM) fungi] directly and indirectly influence the
soil food web through multitrophic feedback loops (Fig. 9.1). We highlight the “state of the
art,” identify knowledge gaps, and propose future research directions.
We postulate three major channels through which photosynthetically derived C is trans-
ferred into the soil food web: via bacteria, fungi, and herbivores (Hunt et al., 1987). The fun-
gal channel consists of saprotrophs in addition to mycorrhizal fungi. Although there is some
debate that some types of mycorrhizal fungi (e.g., EcM fungi) may also function as saprotrophs
(Chapter 20), recent evidence suggests that mycorrhizal fungi do not assimilate C from organic
matter (Lindahl and Tunlid, 2015) and should be considered a distinct C channel of the food
web. Because more than 80% of terrestrial vascular plant species are associated with mycor-
rhizal fungi and up to 30% of photosynthate is allocated to these symbionts (Wang and Qiu,
2006; Smith and Read, 2008), it is plausible to assume that soil food webs in any given terrestrial
ecosystem derive energy via one or multiple types of mycorrhizal fungi to some degree.
FIGURE 9.1 Simplified food web including the dead (green arrows) and live (blue arrows) organic matter channels.
For simplicity, examples of organisms that directly interact with plants or plant litter, although not necessarily primary
producers (i.e., Enchytraeids, plant feeding nematodes, bacteria, and fungi), were placed in level 1. Illustrations by
Angeline Castilloux (Algoma University Fine Arts Student).
Mycorrhizal fungi penetrate the roots of plants to extract carbohydrates through a mutu-
alistic symbiosis. Mutualism was favored in the process of mycorrhizal evolution in a way
that the fungal partner must provide mineral nutrients and potentially other benefits in
exchange for the C received (Bever et al., 2009; Kiers et al., 2011; Bever, 2015; Argüello et al.,
2016). Consequently, mycorrhizal fungi are intrinsically tied to the host plant at the base of
the trophic chain, having direct and indirect effects on soil food webs. Second trophic-level
organisms in the rhizosphere and hyphosphere can directly consume mycorrhizal biomass.
Indirect effects on the food web include biotic interactions associated with the stimulation
of net primary productivity through enhanced plant nutrition, physiology, and facilitation
of other plant-associated symbioses. Indirect effects also extend to trophic levels III and IV
rhizosphere and hyphosphere biota that do not directly feed on mycorrhizal roots or fun-
gal hyphae (Fig. 9.1). These organisms may access C compounds in exudates and promote
plant (Lugtenberg and Kamilova, 2009) and fungal growth responses (Frey-Klett et al., 2007).
Another indirect effect is that mycorrhizal fungi promote soil aggregation (Miller and Jastrow,
2000; Wilson et al., 2009; Rillig et al., 2010) that provides diverse habitats for soil biota. This
chapter explores these indirect and direct effects in the context of the soil food web, including
multitrophic soil feedback loops. We start by focusing on mycorrhizal effects on net primary
productivity, including specific effects on plant growth and physiology with consequences
on the soil food web.
9.1.1 Mycorrhizas and Net Primary Productivity
“Net primary production (NPP) is the difference between total photosynthesis and total
respiration in an ecosystem” and is estimated by quantifying the new organic matter formed
and retained by living plants in a given time (Clark et al., 2001). Even though primary pro-
duction transferred below-ground is often larger than that kept above-ground (Jackson et al.,
1997), few studies account for the below-ground components of NPP, including mycorrhizal
fungi (Long and Hutchin, 1991; Hobbie, 2006; Litton and Giardina, 2008; Clemmensen et al.,
2015; Fernandez et al., 2016). Mycorrhizal fungi may affect processes such as the shedding of
leaves, flowers, and fruits above-ground and root turnover below-ground. These processes
are key to understanding the structure and function of the soil food web but there is little
experimental data available because most studies restrict the quantification of mycorrhizal
effects to total host biomass.
Mycorrhizas affect the soil food web through changes in root architecture, lifespan, and
turnover. They are associated with fine root promotion (e.g., Klein et al., 2016). However,
the turnover of fine roots (<2 mm in diameter) can represent a particularly significant C loss,
exceeding that of leaves (Jackson et al., 1997). Plant biomass is also lost through herbivory,
and likely via volatile organic compounds and leached organic compounds (e.g., allelopathic
compounds). Therefore to account for the net effect of mycorrhizal fungi on NPP there is a
need for studies capable of simultaneously accounting for these multiple processes associ-
ated with biomass losses. In addition, studies must account for total mycorrhizal fungal bio-
mass, including the different types of mycorrhizal fungi co-occurring in ecosystems [consult
Orwin et al. (2011) for a modeling approach and Soudzilovskaia et al. (2015) for a proposed
methodology to account for the contribution of AM and EcM fungi to C cycling]. Typically
studies take into consideration inorganic or organic nutrient uptake via mycorrhizal fungi
but fail to concurrently consider the C transfers between hosts and mycorrhizal fungi (see
Chapter 21). An exception is the study by Orwin et al. (2011) taking into account C transfers
between hosts and EcM fungi and ericoid mycorrhizas while considering mycorrhizal access
to organic nutrients. They demonstrated that under nutrient-limiting conditions, mycorrhizal
mobilization of organic nutrients can result in increased below-ground NPP through greater
host transfer of C to mycorrhizal fungi. Concurrently, increased competition with saprotrophs
may further lead to overall reduced soil respiration (see Section 9.2 and Chapters 23 and 24).
Although it is well established that mycorrhizal colonization affects root biomass (Jonsson
et al., 2001; Lerat et al., 2002), fewer studies have focused on combined effects on root archi-
tecture, turnover, and lifespan. Root lifespan varies according to plant species and is tightly
connected to root architecture. It has been shown that root lifespan varies considerably even
within small root size classes (Wells and Eissenstat, 2001; Tierney and Fahey, 2002). Taking
this into consideration, novel approaches that use branch order have emerged to determine
root turnover rates more accurately (Guo et al., 2008a). Host responses to mycorrhizal fungi
include reductions in root/shoot ratio (Azcon and Ocampo, 1981 as cited by Johnson, 2010)
and, consequently, to potential net reductions in the turnover and decomposition of roots
(Langley and Hungate, 2003). In these cases, mycorrhizal biomass replaces root biomass,
which may change decomposition dynamics. Furthermore, AM fungi have been shown to
significantly reduce root lifespan. This may be the result of the mycorrhizal stimulation of
more branched root systems, which are thinner and therefore more susceptible to degrada-
tion; however, they may also be more suitable to further mycorrhizal colonization (Guo et al.,
2008b). Although the stimulation of root branching by AM fungi has been shown in many
plant species; this is not a consistent response (Péret et al., 2009 and review by McCormack
and Guo (2014)). Moreover, mycorrhizal protection against pathogens and herbivores among
other factors (e.g., increased stress tolerance) may contribute to counteract reductions in root/
shoot ratio (Lewandowski et al., 2013), thereby further complicating calculations on the effect
of mycorrhizas on NPP and, consequently, the soil food web. This is an area requiring further
9.1.2 Mycorrhizas and Plant–Soil Feedback
Plant–soil feedback results from the abiotic and biotic changes imposed by a plant on its
rhizosphere that in turn provide feedback to the plant community (Ehrenfeld et al., 2005;
van der Putten et al., 2013). Plant community diversity depends on the balance between mutual-
istic, competitive, and antagonistic biotic interactions. Concurrently, the diversity of soil biotic
communities depends on plant community diversity (Eisenhauer et al., 2012). Mycorrhizal
fungi have the potential to increase plant diversity and productivity in communities (van der
Heijden et al., 1998; Klironomos et al., 2000; van der Heijden et al., 2008). This may result from
alleviation of plant–plant competition (Wagg et al., 2011) and effects on the temporal dynam-
ics of plant–soil feedback (Bever et al., 2012). In contrast, mycorrhizal fungi may reduce plant
community diversity when the community is dominated by highly mycorrhizal-responsive
species (Hartnett and Wilson, 2002).
AM fungi are not host specific, but soil and plant traits determine AM fungal commu-
nity structure, which may lead either to positive or negative feedback. Positive feedback
contributes to dominance in plant communities and, consequently, to lower plant species
diversity. In contrast, negative feedback is necessary for increased plant diversity in com-
munities. Negative feedback caused by hosts preferentially associating with relatively poor
mycorrhizal growth promoters relative to other co-existing plants is possible (Bever, 2002;
but see Argüello et al., 2016). However, interactions between mycorrhizal fungi, pathogens,
and potentially other enemies in the context of soil and plant traits are key to understand-
ing feedback responses (Wehner et al., 2010; Reininger et al., 2015). Newsham et al. (1995)
showed that the sole function of an AM fungus can be pathogen protection of its host. Since
then, many other studies have shown that host pathogen protection may be an important
trait of mycorrhizal fungi, likely driven by isolate specific traits (Wehner et al., 2010, 2011;
Jung et al., 2012; Lewandowski et al., 2013). Furthermore, pathogen accumulation in rarer
plants may act as a selective pressure for the promotion of positive feedback loops between
mycorrhizal fungi and other groups of beneficial soil biota (Latz et al., 2012). Among these
are endophytes (Brundrett, 2006; Herre et al., 2007; Hardoim et al., 2015; but Mack and
Rudgers, 2008), plant growth promoting bacteria (Artursson et al., 2006; Miransari, 2011),
and N2 fixing bacteria (Bauer et al., 2012; Nguyen and Bruns, 2015). The field of virology is
also starting to explore not only the role of mycorrhizal symbioses on disease-causing plant
viruses (Rúa et al., 2013) but also on the detection of mycoviruses in mycorrhizas (Kitahara
et al., 2014; Ezawa et al., 2015). Recently Ke et al. (2015) used a trait-based approach linking
plant–soil feedback to the interplay between pathogens and mycorrhizal fungi while taking
into consideration plant and microbial traits, including litter quality. They found that the
importance of litter decomposability as a driver of plant–soil feedback was greater when
the relative abundance of mycorrhizal fungi increased because of their positive feedback on
litter production. Future empirical studies should integrate trait-based approaches in the
context of food webs to enable greater predictability regarding the direction of plant–soil
feedback (Kardol et al., 2015).
In this section we focus on the interactions between mycorrhizal fungi, bacteria, and fun-
gal saprotrophs (i.e., organisms that obtain their source of metabolic C from dead organic
matter) (Fig. 9.1). This is critical, given its implications for C sequestration in light of climate
warming. Saprotrophs not only represent a large component of the soil biomass but also play
a key role in soil organic matter (SOM) decomposition and, given that soil represents the
largest terrestrial pool of C, the effect of mycorrhizal fungi on SOM decomposition/stabiliza-
tion is extremely important (Averill et al., 2014). There are two contrasting hypotheses with
regard to the role that mycorrhizal fungi play on decomposition through interactions with
saprotrophs. They can either interact positively through increased C allocation via mycorrhi-
zas into the rhizosphere and hyphosphere or negatively because of competition for resources
such as nutrients, water, and space. The latter hypothesis is gaining more support (see below),
which is consistent with the idea that mycorrhizal fungi contribute to C stabilization in soils.
Furthermore, the more nutrients mycorrhizal fungi are able of accessing from soil, the greater
the SOM stabilization effect via competition with saprotrophs.
AM fungi do not directly decompose or take up any significant amounts of organic mate-
rial (Joner et al., 2000; Nottingham et al., 2013). However, the circumstances whereby AM
fungi may indirectly affect decomposition by increasing or decreasing saprotroph activity
is still an open question in the literature(Chapters 20 and 24). The interplay between pho-
tosynthetic rate, C allocation below-ground, and macronutrient availability in soil is key to
understanding the relationship between AM fungi and saprotrophic activity. Although AM
fungi contribute to the formation of water-stable soil aggregates that may protect SOM from
decomposing (Rillig and Mummey, 2006; Chapter 14), they also grow profusely on patches
of SOM, exerting a physical action as they grow through it that results in a larger surface
area exposed to saprotrophs, which can be carried along the hyphosphere. Voříšková and
Baldrian (2013), have shown that AM fungi increase over time in the leaf litter of a temperate
forest, especially 8 months after the litter was deposited. The greater the C allocation from
hosts into AM fungi, the greater the priming effect (i.e., transient decomposition of relatively
more recalcitrant SOM) via greater saprotrophic activity, which results from the exudation
of energy-rich photosynthates primarily by the roots and turnover of fine roots and hyphae,
leading to the concomitant release of ammonium (and C losses) required to compensate for
the increased plant–AM fungal demand (Cheng et al., 2012; Nuccio et al., 2013). In turn, the
export of ammonium may lead to positive feedback mechanisms for saprotrophs through
AM fungal– mediated changes in enzymatic activity and pH reduction (Bago et al., 1996;
Geisseler et al., 2010). It appears, however, that the priming effect may be transient and driven
primarily by root exudates rather than the direct action of AM fungi (e.g., Hodge, 2014; Koller
et al., 2013a,b; Shahzad et al., 2015; Verbruggen et al., 2016). The importance of this feedback
loop involving ammonium acquisition and transport to hosts in the relationship between AM
fungi and saprotrophs is highlighted by evidence supporting that it has been a strong factor
of evolutionary selection (Cappellazzo et al., 2007; Hodge, 2014).
Whereas increases in C allocation by plants below-ground may contribute to promote
decomposition, AM fungi have been found to reduce the decomposition of certain organic
materials (Leifheit et al., 2015; Verbruggen et al., 2016). This may be linked not only to SOM
recalcitrance and/or high C:N ratio but also to a variety of other potential mechanisms,
including competition for limiting nutrients, localized reductions in water availability
caused by mycorrhizal uptake, the structure of microbial communities present, and tem-
poral aspects either linked to priority effects of microbial introduction or successional pro-
cesses associated with the decomposition process(Chapters 20 and 24). For instance, using
high-throughput molecular methods, Nuccio et al. (2013) demonstrated that the presence
of Glomus hoi hyphae hosted by Plantago lanceolata altered the relative abundances of about
10% of bacterial taxa known as active decomposers (Tanahashi et al., 2005); i.e., Firmicutes
increased and Actinobacteria decreased.
Most of the studies focusing on the interaction between AM fungi and saprotrophic fungi
primarily investigated how their interaction affected the host plants. Once again, effects
of mycorrhizal–saprotrophic interactions can vary in this context. McAllister et al. (1994,
1997) investigated interactions between the AM fungus Glomus mosseae and four species of
saprotrophic fungi, and their resulting effects on host plants, maize (Zea mays) and lettuce
(Lactuca sativa). In both studies, they found that presence of saprotrophic fungi alone did not
affect the biomass of nonmycorrhizal host plants. However, with AM fungal inoculation, the
presence of saprotrophic fungi resulted in smaller plants compared with the mycorrhizal
plants without the saprotrophic fungi. This effect appears to have resulted from AM fungi–
saprotroph competition for nutrients. However, when the AM fungi were inoculated before
introducing saprotrophic fungi, no such significant difference in host plant biomass was
detected and the growth of saprotrophic fungi was smaller. These older studies in combina-
tion with more recent findings (Shahzad et al., 2015; Verbruggen et al., 2016) emphasize the
importance of temporary dynamic interactions between mycorrhizal and saprotrophic fungi
and their host plants.
Understanding the effect of AM fungi on soil microbial community composition is impor-
tant to determine which microbial groups either decompose or stabilize C through AM
fungi–saprobe interactions. Recent studies have established bidirectional compositional
effects between AM fungi and microbial communities (Welc et al., 2010; Leigh et al., 2011).
We propose that the way forward is to adhere to an approach similar to that by Nuccio et al.
(2013); using experimental designs with either individual taxa or plant and indigenous micro-
bial communities and 13C/15N–labeled SOM (e.g., from different natural ecosystems) in a
dual-compartment system (i.e., with a root-free compartment). The use of stable isotopes is
necessary to determine the fate of SOM in the plant host and soil biota. The growth rates
of microbial communities (i.e., those promoted by indigenous AM fungi and utilizing the
SOM) in this dual compartment system need to be determined during the decomposition
process and succession using different molecular incorporation methods (Rousk and Bååth,
2011). At the same time, the use of metagenomic tools can be geared toward providing insight
into ecological function; for example, using both ribosomal and functional genes and tak-
ing advantage of emerging functional databases such as FUNGuild (Voříšková and Baldrian,
2013; Nguyen et al., 2015). Furthermore, in light of increasing evidence on the importance of
local adaptation, using sympatric combinations of soil, mycorrhizal fungi, and plant hosts
is important for ecological relevance or to take advantage of more significant responses that
can emerge from coevolved adaptations between symbiotic partners (Revillini et al., 2016;
Rúa et al., 2016). Given the obligate nature of the mycorrhizal symbiosis and the associated
challenges to establish negative controls in the field, perfecting the use of “rotative cores”
to sever (or not) the hyphae either in the greenhouse or possibly in the field may be one
among other useful approaches to be used in this context (Verbruggen et al., 2016; Brito et al.,
2009). Furthermore, bottom-up and top-down effects need to be taken into consideration. For
instance, the presence of AM fungi was found to significantly change the structure of the sap-
rotrophic fungal community, and the change was amplified when fungivorous Collembola
were present (Tiunov and Scheu, 2005).
Recently, opposing views have emerged in the literature regarding EcM fungi either being
facultative saprotrophs, falling along a biotrophy–saprotrophy continuum (Koide et al.,
2008), or that they are instead decomposers owing to their oxidizing primarily nitrogenous
organic compounds (Lindahl et al., 2007; Chapters 20 and 24). The foundational theory by
Frank (1894) that mycorrhizal fungi play a role as decomposers but are not saprotrophs is
gaining increasing support. Evidence indicates that the evolution of symbiosis has led to the
loss of genes encoding for enzymes involved in the release of metabolically readily available
C compounds in EcM fungi. However, enzymes capable of oxidizing N from organic pools
have been retained. Indeed, there have been a number of in vitro tests demonstrating the
production of lignin-decomposing enzymes by ericoid and EcM fungi (Burke and Cairney,
2002; Courty et al., 2005). Ectomycorrhizal fungi can thus acquire nutrients, primarily N, from
organic material with energy provided by their hosts (Lindahl and Tunlid, 2015). The fate
of C obtained from the hosts and in compounds resulting from EcM fungi decomposition
is an important literature gap, especially considering climate change and C sequestration.
This includes the interactions between mycorrhizal fungi and saprotrophs. By stimulating
photosynthesis, particularly in organic soils (where inorganic N is low), and acting as active
N scavengers, EcM fungi may suppress saprotrophic decomposition and contribute to C
sequestration to a much greater extent than AM fungi (Orwin et al., 2011; Averill et al., 2014).
However, future research should focus on revealing neutral, synergistic, competitive, and
antagonistic interactions between mycorrhizal fungi and different groups of saprotrophs (e.g.,
brown rot fungi, white rot fungi, ligninolytic and nonligninolytic bacteria) either directly or
through modifications of litter quality.
Many soil animals feed directly on live plant roots. They include nematodes (Denton et al.,
1998), Collembola (Endlweber et al., 2009), and insects such as weevils (Gange, 2001), crane-
flies (Treonis et al., 2005), and click beetles (Sonnemann et al., 2012). Root-feeding nematodes
and Collembola live below-ground throughout their lives, whereas most of the root-feeding
insects are soil dwellers only in their juvenile stages (Brown and Gange, 1990). Therefore
direct effects of root-feeding insects on soil food webs are limited to their juvenile stages.
Root-feeding insects can, however, indirectly affect the soil food web by changing plant phys-
iology with resulting effects on mycorrhizal fungi (Johnson and Rasmann, 2015).
Interactions between AM fungi and root-feeding nematodes have been well studied,
mostly for economically important agricultural plants (Hussey and Roncadorl, 1982; Ingham,
1988; Smith, 1988; Pinochet et al., 1996; Roncadori, 1997; Borowicz, 2001; Hol and Cook, 2005;
Schouteden et al., 2015). Most of the studies have focused on beneficial effects of AM fungi
on their host plants against damage by nematodes. Results were, however, mixed and depen-
dent on nematode identity (Ingham, 1988). Root-feeding nematodes can be categorized into
three groups based on their foraging strategies (Schouteden et al., 2015): ectoparasitic nema-
todes stay in the rhizosphere, migratory endoparasitic nematodes migrate and feed inside
of roots, and sedentary endoparasitic nematodes create feeding sites in roots to stay seden-
tary. In a meta-analysis, Borowicz (2001) found that nematodes in general reduce AM fungal
colonization regardless of their feeding types. Conversely, AM fungi tended to have negative
effects on sedentary endoparasitic nematodes but improved the growth of migratory endo-
parasitic nematodes. Among the sedentary endoparasitic nematodes, AM fungi reduced the
abundance of root-knot nematodes more than that of cyst nematodes (Hol and Cook, 2005).
The authors also reported that AM fungi tended to increase the damage caused to roots by
ectoparasitic nematodes compared with nonmycorrhizal control plants. In one of the few
available studies conducted on nonagricultural plants, De La Peña et al. (2006) demonstrated
that AM fungi inoculation of the sand dune grass Ammophila arenaria decreased nematode
colonization and reproduction. This suppression of nematode activity was not caused by
induced systemic resistance (ISR) but by local mechanisms. On the other hand, ISR mediated
by AM fungi has been suggested in some studies as a mechanism to suppress root-feeding
nematodes (Elsen et al., 2008; Hao et al., 2012; Vos et al., 2012a,b).
Interactions between root herbivores and EcM fungi have not been well studied because
most likely, few commercially important agricultural plants host EcM fungi. However, the
increasing number of invasive insects that cause significant mortality of commercially impor-
tant tree species may trigger research in this area (Treu et al., 2014), even if the insects are
primarily leaf-eaters.
Fungivores include nematodes (Hussey and Roncadori, 1981; Ingham et al., 1985; Hua
et al., 2014), protozoa (Petz et al., 1985; Hekman et al., 1992), earthworms (Heděnec et al.,
2013), and microarthropods such as Collembola (Gange, 2000) and mites (Mitchell and
Parkinson, 1976; Schneider et al., 2005) (Fig. 9.1). Soil fungivores are considered the main
drivers of fungal community structure and fungal decomposition processes (Tordoff et al.,
2008; Bardgett et al., 1993; Klironomos and Kendrick, 1995; Filser, 2002). Most research has
concentrated on the negative effect of grazing on mycorrhizal hyphae (Boerner and Harris,
1991; Kaiser and Lussenhop, 1991) and spores (Bakonyi et al., 2002). However, there is some
evidence that mycorrhizal fungi may also actively engage in “chemical warfare” with fungi-
vores to gain privileged access to their nutrients (Klironomos and Hart, 2001; Perez-Moreno
and Read, 2001).
The direct effects of mycorrhizal-feeding fungivores on mycorrhizal fungi and their host
plants depends on their abundance (Finlay, 1985; Harris and Boerner, 1990; Klironomos and
Ursic, 1998; Gange, 2000; Crowther et al., 2012) and can be positive (Lussenhop, 1996), neutral
(Larsen and Jakobsen, 1996; Wurst et al., 2004) or negative (Warnock et al., 1982). In some cases,
effects may be negative for one symbiotic partner and positive for the other (Lussenhop, 1996;
Bakhtiar et al., 2001; Bakonyi et al., 2002; Hua et al., 2014), and the mechanisms for this may
result from complex feedback loops. For example, Lussenhop (1996) interpreted the stimu-
lated growth of mycorrhizal roots by fungivorous Collembola as compensatory growth for the
reduction of mycorrhizas. Alternatively, preferential feeding by Collembola and other fungi-
vores on saprotrophic fungi over mycorrhizal fungi can provide indirect positive feedback to
mycorrhizal fungi (Green et al., 1999; Gange, 2000; Lindahl et al., 2001). For example, Crowther
et al. (2013) showed that the presence of fungivorous isopods that preferentially fed on basid-
iomycete fungi increased the relative abundances of AM and other fungi. The increased fun-
gal diversity associated with the presence of isopods promoted enzymatic activity linked to
mineralization. Similarly to AM fungi, under certain conditions (e.g., at relatively low den-
sities) fungivores can have positive effects on the host (Ek et al., 1994). In addition, Kaneda
and Kaneko (2004) found that a Collembola species, Folsomia candida, preferred EcM fungal
hyphae cut from the root 56 h before feeding than freshly cut hyphae. This result indicates
that Collembola may preferentially feed on dead mycorrhizal hyphae, thereby enhancing
host-nutrient availability.
Understanding the community structure of fungivores combined with their feeding pref-
erences for either mycorrhizal fungi or saprotrophs is important to predict SOM turnover
caused by the competitive interactions between these two groups. Studies on these interac-
tions are still sparse and have emphasized AM fungi (but Hiol et al., 1994; Kanters et al., 2015).
Many studies have demonstrated that Collembola (Bardgett et al., 1993; Hiol et al., 1994;
Klironomos and Ursic, 1998; Klironomos et al., 1999; Gange, 2000; Scheu and Simmerling,
2004; Heděnec et al., 2013), nematodes (Hasna et al., 2007), mites (Maraun et al., 2011), and
earthworms (Bonkowski et al., 2000) have preferential feeding for saprotrophic fungal taxa
rather than mycorrhizal fungi, which may in some cases only serve as choice of last resort
(e.g., Schreiner and Bethlenfalvay, 2003). Nevertheless, mycorrhizal-feeding fungivores may
contribute to regulate the flow of photosynthates below-ground from mycorrhizal plants
(Johnson et al., 2005). 13C/15N-labeling methods have suggested that photosynthesized C
enters fungivores via grazing on EcM fungal hyphae (Pollierer et al., 2012). But again, this
C pathway may not be the most important part of their diet (Potapov and Tiunov, 2016).
Conversely, Schneider et al. (2005) demonstrated that the most preferred fungal types by
three species of oribatid mites (Carabodes femoralis, Nothrus silvestris and Oribatula tibialis)
included ericoid mycorrhizal fungi (Hymenoscyphus ericae), EcM fungi (Boletus badius), and
saprotrophic fungi (Alternaria alternata) when given choices of 10 fungal species, including
six EcM fungi, one ericoid fungus, and three saprotrophic fungal species. However, feeding
preferences and selectiveness significantly differed among the three mite species, indicating
that it is challenging to generalize feeding preferences for fungivorous mites.
A general limitation of fungivore feeding-preference experiments is that many species are
polyphagous and can even feed on live roots and litter (Endlweber et al., 2009; Schreiner
and Bethlenfalvay, 2003). Therefore the array of resources presented can be limiting by not
representing the full spectrum of choices available in natural conditions. For example, some
studies employed only mycorrhizal fungi, leaving no other feeding choices, which can poten-
tially overestimate the negative effect of fungivores on mycorrhizal fungi (e.g., Warnock et al.,
1982; Harris and Boerner, 1990). Schreiner and Bethlenfalvay (2003) observed that Isotoma
species of Collembola preferred AM fungal hyphae of mixed Glomus species to mixed species
of saprotrophic fungi. However, when crop residue was added as an alternative choice, the
Collembola preferentially fed on the crop residue over the two types of mycorrhizal hyphae.
Therefore, when assessing the feeding effects of fungivores on mycorrhizal fungi it is impor-
tant to implement mixed diets and to consider that resources change in space and time (Scheu
and Simmerling, 2004; Staaden et al., 2010).
Mechanisms that modulate fungivore foraging behavior include the use of olfactory cues
to select preferred fungal taxa, alert for toxicity, and as indicators of prior hyphal grazing
(e.g., Staaden et al., 2012). Klironomos et al. (1999) suggested thickness of hyphae and nutri-
tional values as two potential explanations. Collembola and mites prefer thin rather than
thick hyphal segments of AM fungi (Klironomos and Kendrick, 1996), and AM fungal hyphae
tend to be thick and multilayered (Klironomos et al., 1999). Mycorrhizal hyphae and spores
may be less nutritious than those of saprotrophic fungi, which has not been tested. Another
possible explanation is the transfer of secondary metabolites from host plants to mycorrhizal
fungi. Duhamel et al. (2013) demonstrated that when host plants (P. lanceolata) were exposed
to fungivorous Collembola, catalpol, a secondary metabolite, was transferred from the plants
to AM fungal hyphae and that hyphal biomass was not significantly affected. Additional data
indeed show that mycorrhizal networks are conduits for the transfer of allelopathic com-
pounds in soil (Barto et al., 2011; Achatz et al., 2014). Some mycorrhizal fungi have evolved
diffusible compounds that are toxic to plants and soil biota (Kempken and Rohlfs, 2010).
Streiblová et al. (2012) described the volatile organic compounds emitted by truffles such
as Tuber melanosporum, which allow them to exclude competing biota from areas defined as
brûlé (i.e., burnt), meaning that it is lacking plants and many members of soil biota. Martin
et al. (2008) found a family of proteins, including one with a snake toxin–like domain, in a
genome analysis of the EcM fungi Laccaria bicolor. Using microcosms, Klironomos and Hart
(2001) demonstrated that F. candida Collembola died after exposure to L. bicolor and that the
carcasses were internally infected by the fungus, which extracted N from the carcasses and
mobilized it to their host plant, Pinus strobus. Conversely, another EcM fungus, Cenococcum
geophilum, isolated from the same study site did not show any evidence of toxicity for the
Collembola. How widespread toxicity is among mycorrhizal fungi is an area requiring more
The feeding choices of fungivores can affect their reproductive ability (Klironomos and
Ursic, 1998; Staaden et al., 2010; Heděnec et al., 2013). Larsen et al. (2008) investigated how
fungal diets affected reproductive performances of F. candida and Folsomia fimetaria. The fun-
gal diets included two AM fungi (Glomus intraradices and Glomus invermaium), root patho-
genic fungi (Rhizoctonia solani and Fusarium culmorum), and saprotrophic fungi (Penicillium
hordei and Trichoderma harzianum). Overall, AM fungi provided less reproductive success to
the Collembola species than other fungi. For F. fimetaria, the two AM fungi provided the least
reproductive success, but F. candida feeding on G. intraradices had intermediate reproductive
success. These dietary preferences are consistent with findings by Klironomos et al. (1999);
AM fungal species tended to provide less reproductive success to a species of Collembola, A.
alternata, compared with saprotrophic fungal species. Mixed diets, even with low- and high-
quality components, generally benefit Collembola reproduction (Scheu and Folger, 2004).
However, such tendency in Collembola reproductive success with saprotrophic over mycor-
rhizal fungi may not apply to other soil fungivores. Ruess and Dighton (1996) and Ruess
et al. (2000) found that a fungivorous nematode, Aphelenchoides spp., generally reproduced
better on EcM fungal diet than with saprotrophic fungi extracted from a spruce forest soil.
However, Giannakis and Sanders (1990) reported that EcM fungus Laccaria laccata enhanced
the reproduction rates as much as the common mushroom (Agaricus bisporus) for three species
of fungivorous nematodes, but this was not the case for the other five species of EcM fungi.
We propose that future research on mycorrhizal–fungivore interactions should continue to
take advantage of high-throughput metagenomic identification tools (e.g., Anslan et al., 2016)
combined with stable isotope tracking and/or the differential N and C isotope fractionation
signatures associated with the different foraging habits of fungi (Griffith, 2004; Johnson et al.,
2005; Mayor et al., 2009). In addition, little is known about certain groups. For instance, little
is known about fungivorous protozoa feeding on mycorrhizal fungi and only few studies
have focused on mycorrhizal interactions with protozoa in general. Nutrient flows through
bacterivorous protozoa have been deemed more important than through fungivorous proto-
zoa, but this view is changing as studies on the diversity and feeding preferences of fungivo-
rous protozoa emerge (Geisen et al., 2016). In terms of mycorrhizal feedbacks, it is known that
some protozoa can significantly contribute to mobilize N from SOM into AM fungi, whereas
other protozoa in the rhizosphere stimulate photosynthesis through hormonal effects (Koller
et al., 2013b). Future research needs to consider protozoa diversity, including unculturable
species and their differential feeding preference among bacteria and fungal guilds.
One of the most notable implications of mycorrhizas–fungivore interactions is mycorrhizal
dispersal. It has been long recognized that mycorrhizal propagules (i.e., hyphae and spores)
have been found in gut contents, casts, and feces of Collembola (Klironomos and Moutoglis,
1999), mites (Lilleskov and Bruns, 2005), earthworms (Reddell and Spain, 1991; Gange, 1993;
Zaller et al., 2011), and even fungal-feeding mammals (Mangan and Adler, 2002). Mycorrhizal
propagules in casts and feces can be viable to infect potential host trees (Reddell and Spain,
1991; Mangan and Adler, 2002). Klironomos and Moutoglis (1999) observed that Collembola
dispersed AM fungi several centimeters away from the rhizosphere and beyond what AM
fungi could disperse on their own. Mangan and Adler (2002) demonstrated that spiny rats
(Proechimys semispinosus) from islands in Panama feed on AM fungal spores as an alterna-
tive food source when fruits are not available. It is likely that other fungal-consuming soil
macrofauna can disperse AM fungal propagules over long distances at different temporal
scales. Further study of the mechanisms of mycorrhizal dispersal is important to elucidate
both small and large scale patterns of mycorrhizal distribution (Davison et al., 2015).
Soil bacterivores are represented mostly by protozoa and nematodes (Rønn et al., 2012).
They interact with mycorrhizal fungi indirectly, and only few studies have investigated
these interactions and effects on host plants (Trap et al., 2016). Bacterivores in the rhizo-
sphere often increase nutrient availability (comprehensive list in Trap et al., 2016). This
increased nutrient availability can stimulate plant growth (e.g., Ingham et al., 1985; Herdler
et al., 2008; Ekelund et al., 2009) and reproduction (Bonkowski et al., 2001a,b; Krome et al.,
2009). Bonkowski (2004) suggested that rhizosphere bacterivores increase N availability via
the “microbial loop” (Clarholm, 1985) involving complex interactions among plant, bacte-
ria, and bacterivores (but Ekelund et al., 2009). Through meta-analysis, Trap et al. (2016)
found that, overall, the presence of bacterivores in the rhizosphere increased shoot and
root biomass by over 20% compared with controls without bacterivores, with no significant
change in shoot/root ratio.
Studies investigating interactions among host plants, bacterivores, AM fungi (Herdler
et al., 2008; Koller et al., 2013a,b; but Wamberg et al., 2003a,b), and EcM fungi (Jentschke et al.,
1995; Setälä et al., 1999; Bonkowski et al., 2001a,b; Irshad et al., 2012) indicate that the presence
of both mycorrhizal fungi and bacterivores results in increased above-ground production of
the host plants (Trap et al., 2016). The presence of AM fungi can reduce bacterivore popula-
tions (e.g., Wamberg et al., 2003a) by decreasing root exudation (Meier et al., 2013) and/or
lateral root production (Jentschke et al., 1995; Bonkowski et al., 2001a,b; Herdler et al., 2008),
which in turn can reduce bacterial populations. However, the potential counteracting effects
between mycorrhizal fungi and bacterivores on root physiology, biomass, and architecture
appear to still lead to a net positive effect in regard to stimulation of plant above-ground
performance when both groups are present (Trap et al., 2016). Bonkowski et al. (2001a,b)
postulated that plants might allocate their resources to optimize simultaneous exploitation
of plant–mycorrhizal mutualism as well as beneficial effects of bacterivores via the microbial
loop. Indeed, Koller et al. (2013a,b) demonstrated that the presence of both bacteria-feeding
protozoa and AM fungi created an additive positive effect, resulting in significantly higher
above-ground plant growth than presence of either protozoa or AM fungi alone.
Only few studies have specifically focused on reciprocal effects between EcM fungi and
bacterivores, and the results are inconclusive; Jentschke et al. (1995) reported that the pres-
ence of EcM fungi increased the number of bacterivores. In contrast, Irshad et al. (2012) found
that EcM fungi caused reductions in both bacteria and bacterivore nematodes.
In conclusion, positive feedback loops among plant host, mycorrhizal fungi, and bacteriv-
ores appear to be prevalent. However, more ecologically relevant studies are needed to reveal
how mycorrhizal fungi and bacterivores affect each other.
Soil food webs are considered to be donor-controlled systems; the resource density con-
trols consumer density, but the reverse does not occur, especially for fungi (Persson et al.,
1996); thus basal resources, including mycorrhizal fungi, are not considered to be affected
by soil animals at higher trophic levels. For instance, Mikola and Setälä (1998) could not
find evidence of top-down trophic cascades on microbial biomass in a soil microcosm
experiment using soil food webs up to the third level with a predatory nematode species.
However, Bengtsson et al. (1996) suggest that there are empirical and theoretical grounds
to challenge the concept. More and more studies support that top-down trophic cascades
can be significant enough to influence biomass and structure of soil microbes, including
mycorrhizal fungi as well as plants. One example was demonstrated by Bradford et al.
(2002) using different animal size classes to manipulate functional groups to partly reflect
their trophic levels (Turnbull et al., 2014). Their objective was to investigate food web effects
on various ecological functions, including mycorrhizal and plant community composition.
Bradford et al. (2002) found that microcosms including soil animals in all the size classes
significantly reduced AM fungal colonization and root biomass compared with those with-
out macrofauna, indicating a top-down trophic cascade to basal resources including roots
and associated mycorrhizal fungi. However, the manipulation of soil animals by size did
not affect NPP or net ecosystem productivity, most likely because positive and negative
effects of the manipulations canceled each other out. This indicates that interactions among
plants, mycorrhizal fungi, and soil animals in multiple trophic levels in a food web can
be complex, and specific interactions between trophic levels involving mycorrhizal fungi
described in the previous sections can be obscured by other interactions caused by differ-
ent groups in the soil food web. This was suggested by Bradford et al. (2002) and Ladygina
et al. (2010); effects of one functional group can be canceled out by another group in com-
plex trophic interactions of soil food webs, resulting in similar overall plant productivity
among treatments with different combinations of functional groups.
Effects of soil food web community on plant performance (e.g., NPP) is often a primary inter-
est in many soil food web studies, especially those related to agricultural plants (e.g., McAllister
et al., 1997). However, many other ecosystem processes, including nutrient mineralization,
SOM formation, greenhouse gas fluxes, and soil moisture retention, are also essential ecosystem
services to humanity (Wall et al., 2012). Thus biodiversity in a soil food web and associated
complex interactions and feedbacks among various players, including mycorrhizal fungi
and animals at higher trophic levels, in the web should contribute to “ multifunctionality”
(Maestre et al., 2012); an ecosystem can maintain various functions, and its below-ground food
web is a critical component for all the functions (Barrios, 2007). The importance of diversity
in soil food webs, including mycorrhizal fungi, for multifunctionality was demonstrated by
Wagg et al. (2014). By manipulating soil food web structure using different size classes of soil
organisms in a manner similar to that by Bradford et al. (2002), Wagg et al. (2014) showed
that biodiversity of soil food webs controlled many ecosystem functions, and the biodiversity
and multifunctionality indices were significantly correlated with each other. This is consis-
tent with the result of a study by de Vries et al. (2013), which demonstrated that soil food
web properties were significant predictors of ecosystem processes, including C and N cycling
across European land use systems. Given the evidence to support that mycorrhizal fungi play
major roles in soil food webs, mycorrhizal fungi must significantly contribute to ecosystem
More than a decade ago, Scheu (2002) suggested two lines of research as important to
advance soil food web ecology in the future: the adoption of new methodologies and better
experimentation, including more food web components. The first suggestion has been well
implemented; new technologies in molecular and stable isotope methods have contributed
to our understanding of soil food web ecology (Traugott et al., 2013). For instance, advances
in molecular methods such as high-throughput sequencing and bioinformatics have helped
us better understand the community structure of soil microbes, including mycorrhizal fungi,
which are the basal resources in soil food webs (e.g., Nuccio et al., 2013; Crowther et al., 2013).
One future application of high-throughput sequencing can be the investigation of microbivore
diets. For instance, it can be used to investigate gut contents of fungivores (e.g., Collembola
and earthworms) to explore the relative importance between saprotrophic and mycorrhizal
fungi as food sources (Remén et al., 2010; Greenstone et al., 2012).
Advances and popularity of stable isotope analyses for C and N have helped us under-
stand energy and nutrient flow through soil food webs (e.g., Pollierer et al., 2007) and assess
food web compartmentalization and trophic levels (Pollierer et al., 2009; Crotty et al., 2012).
Notable techniques include compound-specific stable isotope analyses of biomarkers such as
phospholipids and neutral and lipid fatty acids (e.g., Olsson and Johnson, 2005; Drigo et al.,
2010; Pollierer et al., 2012). Developing stable isotope instruments such as nanoscale second-
ary ion mass spectrometry (nanoSIMS) (Wagner, 2009; Hatton et al., 2012) can be applied
for soil food web ecology in the future. For instance, nanoSIMS can quantify incorporation
of substrates labeled with stable isotopes (e.g., 13C and 15N) of single microbes and animals
(Musat et al., 2012) such as bacteria (Lechene et al., 2006), cyanobacteria (Ploug et al., 2010,
2011), and zooplankton (Eybe et al., 2009). Thus nanoSIMS can be a promising technology to
reveal energy and nutrient transfer in soil food webs.
In regard to the second suggestion by Scheu (2002), i.e., better experimentation including
more food web components, it has only been implemented to a limited extent. Two studies
using manipulation of functional groups in soil food webs via body sizes by Bradford et al.
(2002) and Wagg et al. (2014) described above (Section 9.6), and a full-factorial experiment
with three different functional groups by Ladygina et al. (2010) are three of the few studies
which strived to assess effects of multiple functional groups on ecosystem processes. Most of
the studies investigating the relationship between mycorrhizal fungi and soil organisms at
higher trophic levels have used simple microcosms or mesocosms with reduced factors. This
reductionist approach is often necessary for theoretical and practical reasons to investigate
specific cause-and-effect relationships among well-defined groups in trophic levels, keeping
experiments manageable with limited resources. However, in the real world, multifaceted
complexity exists in any given soil food web, such as many plant species (both mycorrhizal
and nonmycorrhizal) interacting with multiple mycorrhizal fungal species, various plant spe-
cies of different functional groups at different developmental stages and many more species
of soil organisms at different trophic levels (Beare et al., 1995). A soil food web in a real world
is truly a “tangled bank,” as Charles Darwin (1859) described to emphasize the complexity of
ecosystems in On the Origin of Species. Therefore the interactions and feedbacks among mycor-
rhizal fungi, their host plants, and specific groups in the soil food webs should be interpreted
and viewed in the context of interactivity (Moore et al., 2003). To advance our understanding
of complex interactions among multiple trophic levels in soil food webs and their effects on
ecosystem processes, we need more food web experiments using innovative manipulation
means for functional groups, such as body sizes as employed by Bradford et al. (2002).
An alternative approach to account for complexity in soil food webs is to use casual corre-
lations based on a priori knowledge for observational data, such as de Vries et al. (2013), who
found that food web characteristics were significant predictors for C and N biogeochemistry
in soils. Similar approaches in combination with analytical methods requiring high computa-
tional power such as structural equation models (Grace et al., 2012) will be a future direction
for soil food web ecology.
Another way to contend with the complex nature of dynamics of soil food webs and their
resulting ecosystem functions is modeling. This approach has been used since the 1980s (e.g.,
Hunt et al., 1987; Moore and William Hunt, 1988; Moore et al., 1993; Ke et al., 2015) and con-
tinues to contribute to our understanding of energy and nutrient flows through soil food
webs. Modern computational capacity helps us simulate food web dynamics with reason-
able costs and time and enhance our understanding of complex interactions and feedbacks
among players in a soil food web, including mycorrhizal fungi. For instance, Moore et al.
(2014) added extracellular enzymes and root structure in two-dimensional space in detrital
food webs with two trophic levels to simulate energy dynamics and system stability. Similar
simulation models with more trophic levels are feasible with increasing computational power
with reasonable costs in the future.
This work was funded by an NSERC Discovery Grant and Canada Research Chair to PMA. We are grateful to
Angeline Castilloux and Tiina Keranen for their support designing Fig. 9.1. We are also thankful to Dr. Robert Koller
for his thorough review of our manuscript and valuable feedback.
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... The representation of the soil food web that I used for this thesis (Fig. 2) includes organisms ranging from microorganisms to macrofauna (thus excluding vertebrates and viruses) and includes various types of interactions, e.g., mutualisms, parasitism, predation, which all constitute trophic interactions as they represent a carbon transfer that is needed for the growth and development of the groups in the subsequent trophic levels. For example, plant symbionts such as mycorrhizal fungi are a major component of the soil food web and have a trophic interaction with plants as most of the carbon they obtained comes from this mutualistic association (Antunes & Koyama 2017). ...
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Although soil organisms represent one-quarter of the whole biodiversity on earth, our current understanding of the main drivers of soil biodiversity along environmental gradients is mostly restricted to a limited set of aboveground macro-organisms. In light of increasing global threats to ecosystems, the inclusion of soil organisms into macroecological studies is crucial to improve predictions of ecological responses of terrestrial ecosystems to global changes and support their conservation. Moreover, multitrophic approaches that account for multiple groups of interacting organisms in the ecosystem allow a more holistic understanding of soil biodiversity and its drivers.In my PhD, I aimed at getting a better understanding of the response of soil multitrophic diversity to rapid environmental changes at regional and local scales, by combining soil environmental DNA metabarcoding data, mathematical and statistical tools derived from network theory, and food web ecology.The thesis is developed in four chapters. First, because most of the analyses were based on eDNA metabarcoding data, I needed to gain a better understanding of the uncertainties associated with the use of eDNA metabarcoding in empirical analyses. In the first chapter, I showed that the use of Shannon diversity led to more reliable results from different ecological analyses. I then proposed a roadmap of crucial curation steps for different types of ecological analyses. Second, using eDNA soil data from subarctic birch forests of Northern Norway, I showed that the effect of severe moth outbreaks has cascaded locally from plant communities to the entire soil food web, creating a shift in the ecosystem state. Next, I studied how soil multitrophic diversity responded to environmental gradients using a large-scale biodiversity observatory in the French Alps (chapters 3 and 4). In the third chapter, I conducted a comparative analysis across major soil trophic groups to assess the drivers of soil diversity in the light of well known ecological hypotheses applied to the soil context. I found that the energy and physiological tolerance hypotheses were particularly relevant in predicting the spatial variation in soil biodiversity. Finally, in the fourth chapter, I described how soil food webs structure and composition varied along environmental gradients and in the function of human activities and assessed the main drivers of this variation.I believe my PhD has opened new research avenues in the understanding of multi-trophic soil biodiversity. Zooming out from the species level to a more robust definition of trophic and functional groups allows a larger inclusion of multiple groups and to reach the ultimate goal of understanding all-in-end soil biodiversity distribution and composition.
... This fact may be due to the low nutrient availability (mainly P = 0.10 mg dm −3 ) in the background soil, directing the plant-AMF interaction to actively search for nutrients in the soil. This scenario can reflect in benefits for recovery of a degraded soil, as the joint increase in AMF colonization and root production can drive carbon input into the soil (Rillig et al., 2001), promoting the flow of nutrients and energy between different trophic levels (Antunes & Koyama, 2017). In this way, edaphic conditions can be improved by promoting the establishment of other plant species and contributing to successional advancement and the success of ecological restoration programs. ...
Plant inoculation with Arbuscular mycorrhizal fungi (AMF) can be a useful tool to overcome challenges in dry forest restoration. However, advances are still needed to guide choices regarding soil origin and inoculum production methods, since outcomes can vary due to plant‐soil feedbacks (PSF). We evaluate how soil origin and host plant used for inoculum production affect AMF community and therefore the plant biomass accumulation and functional traits. In the conditioning phase, we investigated whether soils originating from a recovered area (Quarry) and a vegetation fragment (Caatinga) would have their AMF communities modified due to the growth of Sorghum bicolor (used for inoculum production) and Senna uniflora (used in Brazilian semiarid restoration). In the feedback phase, we compared the performance of four plants species growing on a degraded soil and inoculated or not by a mixture of AMF isolates in comparison to soil inoculum prepared from the conditioning phase. The inoculum from Caatinga presented seven times more AMF species compared to that from the Quarry, which presented ruderal and stress tolerant species. The soil inoculum conditioned by S. uniflora, regardless of origin, presented greater evenness compared to the soil inoculum produced with S. bicolor and promoted 33% more plant biomass compared to the control without inoculation. Root colonization by AMF increased PSF and decreased plant investment in functional traits such as specific root length (SRL) and specific leaf area (SLA). Our results demonstrate the importance of adopting strategies that preserve local adaptation of inoculants produced. The use of native plant for propagation of native AMF in the conditioning phase provided more positive responses for Mesosphaerum suaveolens and Rhaphiodon echinus than inoculated with introduced AMF isolates. This is probably due to the interaction of inoculated plants with responsive AMF present in the soil. Synthesis and applications: Our study shows that conditioning field‐collected soil with S. uniflora and using it for inoculation can be a simple technique to promote biomass accumulation for other native herbaceous species. This preserves the compatibility between the soil inoculum produced with native AMF and native plants, representing an important tool for restoration programs.
... One gram of soil is typically inhabited by more than 4 × 10 3 bacterial species [34][35][36][37][38], and this considerable diversity plays a pivotal role in ecosystem services involved in, to name a few, the biogeochemical cycling of elements, soil formation and interaction with macro-organisms (i.e. plants, soil fauna) [39][40][41][42][43]. Furthermore, freshwater and marine sediments are considered to be hotspots of bacterial diversity [44][45][46]; the top 50 cm of marine sediments can contain ~ 1 × 10 29 bacterial species [47][48][49][50]. ...
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Heavy metal (HM) accumulation in soil affects plants and soil fauna, yet the effect on microbial alpha-diversity remains unclear, mainly due to the absence of dedicated research synthesis (e.g. meta-analysis). Here, we report the first meta-analysis of the response of soil microbial alpha-diversity to the experimental addition of cadmium (Cd) and copper (Cu). We considered studies conducted between 2013 and 2022 using DNA metabarcoding of bacterial and fungal communities to overcome limitations of other cultivation- and electrophoresis-based techniques. Fungi were discarded due to the limited study number (i.e. 6 studies). Bacterial studies resulted in 66 independent experiments reported in 32 primary papers from four continents. We found a negative dose-dependent response for Cu but not for Cd for bacterial alpha-diversity in the environments, only for Cu additions exceeding 29.6 mg kg ⁻¹ (first loss of − 0.06% at 30 mg kg ⁻¹ ). The maximal loss of bacterial alpha-diversity registered was 13.89% at 3837 mg kg ⁻¹ . Our results first highlight that bacterial communities behave differently to soil pollution depending on the metal. Secondly, our study suggests that even extreme doses of Cu do not cause a dramatic loss in alpha-diversity, highlighting how the behaviour of bacterial communities diverges from soil macro-organisms. Graphical abstract
... Although there is considerable concern that inoculation with a novel species or genotype that is not locally co-adapted may result in population-level changes, there is a lack of data on the potential long-term alterations to native AM fungal communities following inoculation with commercial bioinoculants. If these changes in AM fungal communities result in functional changes, such as losses in soil aggregation, alterations in nutrient uptake, or shifts in soil microbial biodiversity, ecosystem functioning may also be adversely affected [52,54,[58][59][60]. ...
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There has been a surge in industries built on the production of arbuscular mycorrhizal (AM) fungal-based inoculants in the past few decades. This is not surprising, given the positive effects of AM fungi on plant growth and nutritional status. However, there is growing concern regarding the quality and efficacy of commercial inoculants. To assess the potential benefits and negative consequences of commercial AM fungal inoculants in grasslands, we conducted a controlled growth chamber study assessing the productivity and AM fungal root colonization of nine grassland plant species grown in grassland soil with or without one of six commercial AM fungal products. Our research showed no evidence of benefit; commercial inoculants never increased native plant biomass, although several inoculants decreased the growth of native species and increased the growth of invasive plant species. In addition, two commercial products contained excessive levels of phosphorus or nitrogen and consistently reduced AM fungal root colonization, indicating an unintentional de-coupling of the symbiosis. As there is little knowledge of the ecological consequences of inoculation with commercial AM fungal products, it is critical for restoration practitioners, scientists, and native plant growers to assess the presence of local AM fungal communities before investing in unnecessary, or possibly detrimental, AM fungal products.
... We found that LC-excess, but not SW-excess, was more negative for plants that have been shown to form mycorrhizal associations with either arbuscular or ectomycorrhizal fungi. Mycorrhizal associations are beneficial for the host plant because they increase nutrient and water availability for the plant and in return, the host plant supplies carbohydrates to their mycorrhizal partner (Antunes and Koyama, 2017). Given the carbon costs of these associations for the plant, to maximise their investment return, we would expect that plants forming mycorrhizal associations would allocate larger proportions of their root and fungal hyphal biomass to the shallower soil layers where nutrient concentrations are higher (Esteban and Robert, 2001). ...
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Isotope-based approaches to study plant water sources rely on the assumption that root water uptake and within-plant water transport are non-fractionating processes. However, a growing number of studies have reported offsets between plant and source water stable isotope composition for a wide range of ecosystems. These isotopic offsets can result in the erroneous attribution of source water used by plants and potential overestimations of groundwater uptake by the vegetation. We conducted a global meta-analysis to quantify the magnitude of these plant source water isotopic offsets and explored whether their variability could be explained by either biotic or abiotic factors. Our database compiled 112 studies spanning arctic to tropical biomes that reported the dual water isotope composition (δ2H and δ18O) of plant (stem) and source water, including soil water (sampled following various methodologies and along a variable range of depths). We calculated plant source 2H offsets in two ways: a line conditioned excess (LC-excess) that describes the 2H deviation from the local meteoric water line and a soil water line conditioned excess (SW-excess) that describes the deviation from the soil water line, for each sampling campaign within each study. We tested for the effects of climate (air temperature and soil water content), soil class, and plant traits (growth form, leaf habit, wood density, and parenchyma fraction and mycorrhizal habit) on LC-excess and SW-excess. Globally, stem water was more depleted in 2H than in soil water (SW-excess < 0) by 3.02±0.65 ‰ (P < 0.05 according to estimates of our linear mixed model and weighted by sample size within studies). In 95 % of the cases where SW-excess was negative, LC-excess was negative, indicating that the uptake of water that had not undergone evaporative enrichment (such as groundwater) was unlikely to explain the observed soil–plant water isotopic offsets. Soil class and plant traits did not have any significant effect on SW-excess. SW-excess was more negative in cold and wet sites, whereas it was more positive in warm sites. The climatic effects on SW-excess suggest that methodological artefacts are unlikely to be the sole cause of observed isotopic offsets. Our results would imply that plant source water isotopic offsets may lead to inaccuracies when using the isotopic composition of bulk stem water as a proxy to infer plant water sources.
... Otherwise, a negative interaction between ectomycorrhizal fungi and phytophagous fungi could explain the decrease in diversity of the latter (Figure 4a). Indeed, ectomycorrhizal fungi can provide protection against pathogens to their plant hosts, thus reducing the incidence of phytophagous fungi and their diversity (Antunes & Koyama, 2017;Wang et al., 2019). ...
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Aim Although soil biodiversity is extremely rich and spatially variable, both in terms of species and trophic groups, we still know little about its main drivers. Here, we contrast four long‐standing hypotheses to explain the spatial variation of soil multi‐trophic diversity: energy, physiological tolerance, habitat heterogeneity and resource heterogeneity. Location French Alps. Methods We built on a large‐scale observatory across the French Alps (Orchamp) made of seventeen elevational gradients (~90 plots) ranging from low to very high altitude (280–3,160 m), and encompassing large variations in climate, vegetation and pedological conditions. Biodiversity measurements of 36 soil trophic groups were obtained through environmental DNA metabarcoding. Using a machine learning approach, we assessed (1) the relative importance of predictors linked to different ecological hypotheses in explaining overall multi‐trophic soil biodiversity and (2) the consistency of the response curves across trophic groups. Results We showed that predictors associated with the four hypotheses had a statistically significant influence on soil multi‐trophic diversity, with the strongest support for the energy and physiological tolerance hypotheses. Physiological tolerance explained spatial variation in soil diversity consistently across trophic groups, and was an especially strong predictor for bacteria, protists and microfauna. The effect of energy was more group‐specific, with energy input through soil organic matter strongly affecting groups related to the detritus channel. Habitat and resource heterogeneity had overall weaker and more specific impacts on biodiversity with habitat heterogeneity affecting mostly autotrophs, and resource heterogeneity affecting bacterivores, phytophagous insects, enchytraeids and saprotrophic fungi. Main Conclusions Despite the variability of responses to the environmental drivers found across soil trophic groups, major commonalities on the ecological processes structuring soil biodiversity emerged. We conclude that among the major ecological hypotheses traditionally applied to aboveground organisms, some are particularly relevant to predict the spatial variation in soil biodiversity across the major soil trophic groups.
... These probabilities define how likely it is that a connection exists between any two species belonging to the two connected groups, and they were guessed from information available in the literature (Table S3 and "Groups_Pint_REV.csv" in Appendix S1). For example, there is mixed evidence about the specificity of relationships between plants and mycorrhizal fungi (Antunes & Koyama, 2017). In uncertain cases like this, we used a probability of 0.5. ...
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This is an open access article under the terms of the Creat ive Commo ns Attri bution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. Abstract Ecologists have long debated the properties that confer stability to complex, species-rich ecological networks. Species-level soil food webs are large and structured networks of central importance to ecosystem functioning. Here, we conducted an analysis of the stability properties of an up-to-date set of theoretical soil food web models that account both for realistic levels of species richness and the most recent views on the topological structure (who is connected to whom) of these food webs. The stability of the network was best explained by two factors: strong correlations between interaction strengths and the blocked, nonrandom trophic structure of the web. These two factors could stabilize our model food webs even at the high levels of species richness that are typically found in soil, and that would make random systems very unstable. Also, the stability of our soil food webs is well-approximated by the
... protists) were not considered as prey of other free living predators, and (3) feeding preferences, e.g. fungivores fed only on saprotrophic fungi and Ectomycorrhizal, which are preferred to arbuscular mycorrhizal fungi 75 . The complete metaweb of trophic groups can be found in Supplementary Fig. 1 and the adjacency matrix is available in Supplementary files. ...
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The increasing severity and frequency of natural disturbances requires a better understanding of their effects on all compartments of biodiversity. In Northern Fennoscandia, recent large-scale moth outbreaks have led to an abrupt change in plant communities from birch forests dominated by dwarf shrubs to grass-dominated systems. However, the indirect effects on the belowground compartment remained unclear. Here, we combined eDNA surveys of multiple trophic groups with network analyses to demonstrate that moth defoliation has far-reaching consequences on soil food webs. Following this disturbance, diversity and relative abundance of certain trophic groups declined (e.g., ectomycorrhizal fungi), while many others expanded (e.g., bacterivores and omnivores) making soil food webs more diverse and structurally different. Overall, the direct and indirect consequences of moth outbreaks increased belowground diversity at different trophic levels. Our results highlight that a holistic view of ecosystems improves our understanding of cascading effects of major disturbances on soil food webs.
... The phylum Glomeromycota includes a large number of arbuscular mycorrhizal fungi (AMF), which can enhance nutrient availability for plants (van der Heijden et al., 2015). It has been shown that predation by soil fungivorous nematodes and protists contributes to turnover and changes in the structure of the AMF community (Chakraborty et al., 1985;Antunes and Koyama, 2017), thereby impacting plant phosphorus uptake and crop yield . The random forest analysis and multiple stepwise regression showed that protist diversity, OTU richness and community composition explained more variation in the beta diversity of certain saprotrophic fungi (e.g., Geomyces and Craterocolla) than abiotic factors (Fig. 5) (Bodeker et al., 2009;Stursova et al., 2012). ...
Soil fungi have important functions in agricultural ecosystems. They promote crop growth by driving soil nutrient cycling and by forming mycorrhizal symbioses with crop species. Most studies on soil fungi have focused on detecting the edaphic factors that structure fungal communities, but little is known about how climate influences the soil microbiome. Moreover, a profound understanding of how soil fungal communities are modulated by other soil organisms, such as protist predators, is lacking. We investigated the spatial succession of fungal assemblages in China and their potential predator-prey relationships with protists across four climatic zones using 18S rDNA amplicon sequencing. Although stochastic processes dominated the assembly of fungal communities, deterministic drivers of community assembly were more important in high-latitude climatic zones (that is, in the temperate and continental zones) than in low-latitude climatic zones (that is, in the tropics and subtropics). Random forest and variation partitioning analyses showed that biotic effects influenced fungal communities as much as abiotic effects. Biotic factors were better predictors of the abundance of several saprophytic and mycorrhizal fungi than abiotic factors. This finding was further supported by a network analysis, which indicated that the intensity of fungi-protist interactions may stimulate the divergence of prey fungal communities. Our results reveal for the first time the nonnegligible effects of biotic factors on soil fungal community assembly across substantially different climatic zones. The biological mechanisms underlying these effects can be well understood within a predator-prey relationship framework in which protists exert strong top-down control on fungal communities.
Mycorrhizae are mutualisms between plants and fungi that evolved over 400 million years ago. This symbiotic relationship commenced with land invasion, and as new groups evolved, new organisms developed with varying adaptations to changing conditions. Based on the author's 50 years of knowledge and research, this book characterizes mycorrhizae through the most rapid global environmental changes in human history. It applies that knowledge in many different scenarios, from restoring strip mines in Wyoming and shifting agriculture in the Yucatán, to integrating mutualisms into science policy in California and Washington, D.C. Toggling between ecological theory and natural history of a widespread and long-lived symbiotic relationship, this interdisciplinary volume scales from structure-function and biochemistry to ecosystem dynamics and global change. This remarkable study is of interest to a wide range of students, researchers, and land-use managers.
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Carbon trading between adult trees Competition between individual plants for resources is well known, but sharing of resources may also occur. Klein et al. observed tree-to-tree carbon shuttling between roots of tall trees in a mixed temperate forest in Switzerland (see the Perspective by van der Heijden). By applying stable carbon isotope labeling to individual tree canopies, they show that up to 40% of the carbon in the fine roots of one individual may be derived from photosynthetic products of a neighbor. Carbon transfer of this kind, mediated by plant-associated fungi, or mycorrhizae, in the soil, has been reported on a smaller scale in seedlings, but not before in trees. Science , this issue p. 342 ; see also p. 290
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1. The plant-soil feedback (PSF) framework has become an important theory in plant ecology, yet many ecological and evolutionary factors that influence PSFs have yet to be fully considered. Here, we discuss the importance of local adaptation among plants and root-associated fungi and bacteria. Furthermore, we show how inclusion of the optimal resource allocation model can help predict the direction and outcome of PSFs under environmental change. 2. Plants and associated soil microbes have coevolved for millennia, generating adaptations to each other and to their local environment. This local co-adaptation is likely generated by a suite of multi-directional exchanges of goods and services among plants, fungi and bacteria, and the constant changes in aboveground-belowground interaction. 3. Resource limitation may be a driver of local adaptation among organisms involved in nutritional symbioses. The optimal resource allocation (OA) model states that when an essential resource is limited, natural selection will favor taxa that forage optimally by adjusting their biomass and energy allocation such that productivity is equally limited by all resources. Co-adaptation will therefore respond to the local limiting resource conditions through taxa-specific resource transfer interactions. 4. The OA model can help predict the outcomes of PSFs across a range of resource gradients and environmental changes such as increasing drought or atmospheric nitrogen deposition. Positive feedback is predicted in systems where resource exchange among plants and associated soil microbes can ameliorate resource limitation, or in systems where microbes provide another important service such as pathogen defense. Feedback strength is expected to diminish as resources become less limiting. Negative feedback is predicted when resources are in luxury supply and populations of opportunistic plant pathogens increase relative to commensal or mutualist microbes. 5. Future, field-based studies that integrate naturally co-occurring systems of plants, microbes and their local soil are needed to further test the hypothesis that resource availability is an effective predictor of the direction and magnitude of PSFs. A more mechanistic understanding of PSFs will help land managers and farmers to manipulate plant-microbial-soil interactions to respond to environmental change and to effectively harness beneficial symbioses for plant nutrition and pathogen control.
Patterns of fungal spore dispersal affect gene flow, population structure and fungal community structure. Many Basidiomycota produce resupinate (crust-like) basidiocarps buried in the soil. Although spores are actively discharged, they often do not appear to be well positioned for aerial dispersal. We investigated the potential spore dispersal mechanisms of one exemplar of this growth form, Tomentella sublilacina. It is a widespread ectomycorrhizal fungus that sporulates in the soil organic horizon, can establish from the spore bank shortly after disturbance, but also can be a dominant species in mature forest stands. We investigated whether its spores could be dispersed via spore-based food webs. We examined external surfaces, gut contents and feces from arthropod fungivores (mites, springtails, millipedes, beetles, fly larvae) and arthropod and vertebrate predators (centipedes, salamanders) from on and around T. sublilacina sporocarps. Spore densities were high in the guts of many individuals from all fungivore groups. Centipede gut contents, centipede feces and salamander feces contained undigested invertebrate exoskeletons and many apparently intact spores. DAPI staining of spores from feces of fungivores indicated that 7–73% of spores contained intact nuclei, whereas spores from predators had lower percentages of intact nuclei. The spiny spores often were lodged on invertebrate exoskeletons. To test the viability of spores that had passed through invertebrate guts we used fecal droppings of the millipede Harpaphe haydeniana to successfully inoculate seedlings of Pinus muricata (Bishop pine). These results indicate the potential for T. sublilacina spore dispersal via invertebrates and their predators in soil food webs and might help to explain the widespread distribution of this species. It is likely that this is a general mechanism of dispersal for fungi producing resupinate sporocarps, indicating a need to develop a fuller understanding of the linkages of soil food webs and spore dispersal.
To determine if conidia of the nematophagous fungus Drechmeria coniospora are subject to predation by soil protozoa, several sandy soils were enriched with 10 9 conidia of this fungus per g dry soil. After incubation of the samples at 20°C for three weeks, a flagellate was detected as the most dominant mycophagous protozoan. Conidia of several fungi, with minimum diameters between 2 and 16 μm, supported growth of this flagellate, irrespective of pigmentation. Bacteria however could not be used for growth, although bacteria and also latex beads of the same size were ingested. This is, to our knowledge, the first report of an obligate mycophagous soil-borne flagellate. The flagellate was able to grow at the expense of the conidia of D. coniospora in liquid culture, with a specific growth rate of about 0.1 h −1 ; the optimum temperature was 20–24°C. Approximately 10 D. coniospora conidia were required for one flagellate division. In sterilized soil, enriched with 10 8 D. coniospora conidia per g dry soil, the specific growth rate was 0.014 h −1 , when the soil was at 50 or 65% of its water-holding capacity (WHC). In drier soil, i.e. 25% WHC, no growth took place. During growth of the flagellate in soil, the number of D. coniospora was reduced by about 20%, which was in the same order of magnitude as expected on the basis of the requirement of 10 D. coniospora conidia for one flagellate division. Since many conidia remained in the soil after growth of the flagellate, we concluded that although the flagellate is an interesting organism, it does not play a very important role in the survival of D. coniospora conidia in the soil.
Background: Local adaptation, the differential success of genotypes in their native versus foreign environment, arises from various evolutionary processes, but the importance of concurrent abiotic and biotic factors as drivers of local adaptation has only recently been investigated. Local adaptation to biotic interactions may be particularly important for plants, as they associate with microbial symbionts that can significantly affect their fitness and may enable rapid evolution. The arbuscular mycorrhizal (AM) symbiosis is ideal for investigations of local adaptation because it is globally widespread among most plant taxa and can significantly affect plant growth and fitness. Using meta-analysis on 1170 studies (from 139 papers), we investigated the potential for local adaptation to shape plant growth responses to arbuscular mycorrhizal inoculation. Results: The magnitude and direction for mean effect size of mycorrhizal inoculation on host biomass depended on the geographic origin of the soil and symbiotic partners. Sympatric combinations of plants, AM fungi, and soil yielded large increases in host biomass compared to when all three components were allopatric. The origin of either the fungi or the plant relative to the soil was important for explaining the effect of AM inoculation on plant biomass. If plant and soil were sympatric but allopatric to the fungus, the positive effect of AM inoculation was much greater than when all three components were allopatric, suggesting potential local adaptation of the plant to the soil; however, if fungus and soil were sympatric (but allopatric to the plant) the effect of AM inoculation was indistinct from that of any allopatric combinations, indicating maladaptation of the fungus to the soil. Conclusions: This study underscores the potential to detect local adaptation for mycorrhizal relationships across a broad swath of the literature. Geographic origin of plants relative to the origin of AM fungal communities and soil is important for describing the effect of mycorrhizal inoculation on plant biomass, suggesting that local adaptation represents a powerful factor for the establishment of novel combinations of fungi, plants, and soils. These results highlight the need for subsequent investigations of local adaptation in the mycorrhizal symbiosis and emphasize the importance of routinely considering the origin of plant, soil, and fungal components.
The mutualism between plants and arbuscular mycorrhizal fungi (AMF) is widespread and has persisted for over 400 million years. Although this mutualism depends on fair resource exchange between plants and fungi, inequality exists among partners despite mechanisms that regulate trade. Here, we use (33) P and (14) C isotopes and a split-root system to test for preferential allocation and reciprocal rewards in the plant-AMF symbiosis by presenting a plant with two AMF that differ in cooperativeness. We found that plants received more (33) P from less cooperative AMF in the presence of another AMF species. This increase in (33) P resulted in a reduced (14) C cost per unit of (33) P from less cooperative AMF when alternative options were available. Our results indicate that AMF diversity promotes cooperation between plants and AMF, which may be an important mechanism maintaining the evolutionary persistence of and diversity within the plant-AMF mutualism.