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Journal ArticleDOI

Parasitism within mutualist guilds explains the maintenance of diversity in multi-species mutualisms

29 Jul 2020-Theoretical Ecology (Springer Netherlands)-Vol. 13, Iss: 4, pp 615-627
TL;DR: It is shown that asymmetric resource exchange between the plant and its fungal guild can lead to indirect parasitic interactions between guild members, and the interaction structure can explain the maintenance of diversity within guilds in the absence of spatial structure and niche-related processes.
Abstract: We consider here mutualisms where there are multiple species sharing a resource supplied by the same partner. If, as commonly assumed, there is competition between the species, then only the superior competitor should persist. Nevertheless, coexistence of multiple species sharing the same mutualistic partner is a widespread phenomenon. Regulation of nutrient exchange, where each species receives resources from the partner in proportion to the strength of the mutualism between the two, has been proposed as the main mechanism for coexistence in multi-species mutualisms involving the transfer of nutrients. Significant arguments, however, challenge the importance of partner selection processes. We present a mathematical model, applied to the arbuscular mycorrhizal symbiosis, to propose an alternative explanation for this coexistence. We show that asymmetric resource exchange between the plant and its fungal guild can lead to indirect parasitic interactions between guild members. In our model, the amount of carbon supplied by the plant to the fungi depends on both plant and fungal biomass, while the amount of phosphorus supplied by the fungi to the plant depends on both plant and fungal biomass when the plant is small, and effectively on fungal biomass only when the plant is large. As a consequence of these functional responses, more beneficial mutualists increase resource availability, and are indirectly exploited by less beneficial species that consume the resource and grow larger than they would in the absence of the better mutualists. As guild mutualists are not competing, competitive exclusion does not occur. Hence, the interaction structure can explain the maintenance of diversity within guilds in the absence of spatial structure and niche-related processes.

Summary (3 min read)

Introduction

  • Within mutualist guilds, the principle of competitive exclusion seems not to apply.
  • In return for these nutrients, the host plant provides carbon to the fungi.
  • One of the most popular explanations for coexistence of multiple fungal species has been regulation of resource exchange (Palmer et al., 2003) .

Formulating a model for a multi-species mutualism

  • To investigate the dynamics of multi-species mutualisms the authors develop a model for the interactions between a host plant and its associated fungal mutualists.
  • The amount of resource exchanged depends on the plant and fungal biomass.
  • The first terms on the right sides of Eqs. (1a) and (1b) describe the gain in plant and fungal biomass per unit time due to the resource received.
  • The relationship between the specific functional forms chosen for these terms is tied to the biology, and discussed in detail in the following section.
  • AM fungi are obligate mutualists with no saprobic ability and cannot survive in the absence of the host plant, so no intrinsic growth term appears in Eq. (1b).

Quantification of resource exchange

  • Nutrient exchange between the host plant and the fungal mutualists occurs inside the plant root cells, where the AM fungi build nutrient exchange zones called 'arbuscules' (Peterson and Guinel, 2000; Wang et al., 2017) .
  • In the model, the authors thus assume a linear relationship between fungal biomass and phosphorus transfer.
  • The choice of the term for carbon transfer in Eq. (3) implies that when multiple mutualists are associated with the same host, each species is supplied with an amount of host carbon per unit time that its proportional to its individual fungal biomass and to the existing plant biomass.
  • Thus, where a fungus lies on the mutualism-parasitism continuum depends on the context provided by the other fungi present (Lekberg and Koide, 2014) .
  • The authors will analyse the model of Eq. ( 1) using both linear stability analysis and numerical simulations.

Mutualism establishment and coexistence

  • As long as these three conditions are satisfied, the two nullclines in the phase plane of Fig. 1 intersect and coexistence is observed (see SI, section 1 for details).
  • Fig. 2 demonstrates how the benefits and costs of the mutualism are distributed across the plant and fungus, as a function of plant or fungal biomass.
  • In the right panel of Fig. 2 , one can see that when plant biomass is small, the gross benefit functional response of the plant is larger than the cost functional response.
  • Condition (iii) is more likely to be satisfied when the covariance between α and β and the mean α are large, and when the variances V ar(α) and V ar(β) are small.
  • Altogether, conditions (i)-(iii) tell us that it is the overall exchange capacity of all mutualists that determines whether coexistence or extinction of the whole guild will be observed.

Indirect parasitism among guild members

  • Fig. 4 compares plant and fungal growth when the plant is associated with a more mutualistic fungus (species 1), a less mutualistic fungus (species 2), or a combination of the two species.
  • When a less mutualistic fungus (species 2) is considered in pairwise association with the plant, the growth rates and final sizes of the plant and the fungus are lowest.
  • The larger the difference in net benefit provided by guild members, the stronger the indirect parasitic interactions.
  • Pairwise indirect interactions among fungal species are parasitic, since the less mutualistic species takes advantage of the plant growth resulting from the benefit provided by the more mutualistic species.
  • The model predicts none of the interactions between the fungi to be competitive, i.e., disadvantageous for both parties.

Discussion

  • Modelling of mutualistic interactions I present a model that allows for stable coexistence of multiple multualists sharing a resource supplied by a single partner, in the absence of niche-based mechanisms, spatial structure, or preferential allocation.
  • In the model, multi-species mutualism establishment depends on the overall net benefit provided by the guild to the partner.
  • As long as the plant receives enough nutrients to support its growth, coexistence of all mutualists is observed.
  • Inevitably, one of the mutualists will be better than the others at obtaining resource from the partner species.
  • On the other hand, symmetric non-saturating resource exchange (corresponding to linear gross benefit (GB) functional responses) results in unlimited growth of both, the mutualists and the partner species (Gause and Witt, 1935; Vandermeer and Boucher, 1978) .

Mutualism-parasitism continuum

  • Experimental work has shown that symbiotic associations are not always necessarily beneficial, but can, under certain circumstances, become parasitic or commensalistic.
  • The nature of the symbiosis may depend on the genotypes of the interacting species or on environmental conditions (Johnson et al., 1997; Lekberg and Koide, 2014) .
  • Here, the authors present a mechanism that causes interactions to change from mutualistic to parasitic when there is a disproportion in plant and fungal biomass, where the more abundant species is exploited by the less abundant one before mutual growth can be observed.
  • It has already been hypothesized that depletion in plant growth may be observed when the carbon cost set by the fungi is not sufficiently compensated by phosphorus transfer (Lekberg and Koide, 2014; Smith and Smith, 2012) .

Indirect parasitism between guild members

  • The authors show that the main form of interaction between guild members is indirect parasitism, and as guild members are not competing, competitive exclusion is not expected to occur.
  • The presence of a more mutualistic species increases plant biomass, and therefore resource availability, for other guild members.
  • Each fungal mutualist exploits all of the other species that are more mutualistic fungi than itself, and at the same time is itself exploited by each of the species that are less mutualistic.
  • The most mutualistic species is exploited by all other species, and the least mutualistic one is not exploited by any.
  • Previous work has proposed that stable coexistence of multiple species sharing a limiting resource can emerge as a consequence of indirect interactions in multitrophic communities (Stanton, 2003; McCann, 2000) .

Experimental work

  • While there is a great deal of work looking at fungal diversity in the microbiome of plants (Husband et al., 2002; Sugiyama et al., 2014) the results are largely focussed on diversity, rather than fungal biomass over time.
  • Hart et al. (2013) found that the abundance of a less mutualistic fungal species is increased by the addition of a better mutualist colonizing the same host plant, and Argüello et al. (2016) showed that a plant receives more phosphorus from a less mutualistic species in the presence of a better mutualist.
  • All of these results are in agreement with model predictions.
  • The contraddiction could be explained by the fact that in the model the authors assume phosphorus supply to be the only benefit provided to the plant by the fungi.

Future directions

  • Asymmetric nutrient exchange is an important part of the dynamics observed in the model.
  • In particular, the authors do not distinguish between plant structure above or below ground, although plants are known to differentially allocate carbon depending on plant size, environmental conditions or AM fungal abundance (Andersen and Rygiewicz, 1991; Rygiewicz and Andersen, 1994) .
  • It is important to note that the model presented here is not spatially explicit, and allows for an indefinite number of mutualists to be associated with the same host plant.
  • Green arrows represent positive effects ('+') , while red arrows represent negative effects on growth ('−').
  • A mutualistic interaction is one in which the two parallel interactions are denoted as ('+', '+'), while a parasitic interaction is one in which one of the parallel interactions is positive and the other is negative ('+','−').

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Parasitism within mutualist guilds explains the
maintenance of diversity in multi-species mutualisms
Maria Martignoni, Miranda Hart, Jimmy Garnier, Rebecca Tyson
To cite this version:
Maria Martignoni, Miranda Hart, Jimmy Garnier, Rebecca Tyson. Parasitism within mutualist guilds
explains the maintenance of diversity in multi-species mutualisms. Theoretical Ecology, Springer 2020,
�10.1007/s12080-020-00472-9�. �hal-03006662�

Parasitism within mutualist guilds explains the maintenance of
diversity in multi-species mutualisms
Maria Martignoni
1
, Miranda M. Hart
2
, Jimmy Garnier
3
, and Rebecca C. Tyson
4
1
Department of Mathematics, University of British Columbia, Kelowna (Canada),
maria.martignonimseya@ubc.ca
2
Department of Biology, University of British Columbia, Kelowna (Canada), miranda.hart@ubc.ca
3
Laboratoire de Math´ematiques (LAMA), CNRS and Universit´e de Savoie-Mont Blanc, Chambery
(France), jimmy.garnier@univ-smb.fr
4
Department of Mathematics, University of British Columbia, Kelowna (Canada),
rebecca.tyson@ubc.ca
November 16, 2020
Abstract
We consider here mutualisms where there are multiple species sharing a re-
source supplied by the same partner. If, as commonly assumed, there is com-
petition between the species, then only the superior competitor should persist.
Nevertheless, coexistence of multiple species sharing the same mutualistic part-
ner is a widespread phenomenon. Regulation of nutrient exchange, where each
species receives resources from the partner in proportion to the strength of the
mutualism between the two, has been proposed as the main mechanism for coex-
istence in multi-species mutualisms involving the transfer of nutrients. Significant
arguments, however, challenge the importance of partner selection processes. We
present a mathematical model, applied to the arbuscular mycorrhizal symbio-
sis, to propose an alternative explanation for this coexistence. We show that
asymmetric resource exchange between the plant and its fungal guild can lead to
indirect parasitic interactions between guild members. In our model, the amount
of carbon supplied by the plant to the fungi depends on both plant and fun-
gal biomass, while the amount of phosphorus supplied by the fungi to the plant
depends on both plant and fungal biomass when the plant is small, and effec-
tively on fungal biomass only when the plant is large. As a consequence of these
functional responses, more beneficial mutualists increase resource availability, and
are indirectly exploited by less beneficial species that consume the resource and
grow larger than they would in the absence of the better mutualists. As guild
mutualists are not competing, competitive exclusion does not occur. Hence, the
interaction structure can explain the maintenance of diversity within guilds in the
absence of spatial structure and niche-related processes.
Keywords : Mutualism, mutualist guilds, coexistence, arbuscular mycorrhizal fungi, in-
direct interactions, mathematical model, ordinary differential equations, functional response,
density-dependent resource exchange.
corresponding author
1

Introduction1
Within mutualist guilds, the principle of competitive exclusion seems not to apply. Indeed,2
within a guild, mutualists occupying closely related niches coexist on the same partner (Palmer3
et al., 2003). This fact presents a paradox: According to the principle of competitive exclusion4
one would expect less beneficial mutualists, i.e., species that provide a lower amount of nutrient5
in return for the benefit received, to dominate and outcompete more beneficial mutualists6
(Palmer et al., 2003; Hardin, 1960). Yet, mutualisms involving only two interacting species7
are relatively rare (Hoeksema and Bruna, 2000; Herre et al., 1999). New evidence has revealed8
that even mutualisms previously thought to be species-specific, such as for example the fig9
tree-fig wasp mutualism, are now recognised to involve a guild of mutualists with very similar10
habits and morphology (Molbo et al., 2003; Pellmyr, 1999; Knowlton and Rohwer, 2003; Herre11
et al., 1999; Hoeksema and Bruna, 2000).12
The arbuscular mycorrhizal (AM) mutualism is another example that is particularly chal-13
lenging to explain. AM fungi exist in the roots of most terrestrial plants (Smith and Read,14
2010). The hyphae of the fungi grow from the plant roots into the soil, where they are able to15
efficiently increase the absorption of nutrients that are limiting to plant growth (e.g., phospho-16
rus). In return for these nutrients, the host plant provides carbon to the fungi. In nature, a17
single host plant often associates with dozens of AM fungal species, many of them functionally18
indistinguishable (Herre et al., 1999; Hoeksema and Bruna, 2000;
¨
Opik et al., 2006). Guild19
members coexist tightly in space within the roots and in the soil (Bennett and Bever, 2009;20
Aldrich-Wolfe, 2007), rarely displaying the patchy distribution typically associated with niche21
differentiation or aggregation (Powell and Bennett, 2016).22
There has been some investigation as to the mechanism for this coexistence. Niche differ-23
ences (Batstone et al., 2018), colonization-competition trade-offs (Smith et al., 2018), spatial24
structure (Wilson et al., 2003), or physio-evolutionary feedbacks (Bever, 2015), can facilitate25
coexistence in trophic communities as well as in multi-species mutualisms. None of these26
mechanisms, however, can explain coexistence of species with a high degree of niche overlap27
in the absence of spatial structure.28
One of the most popular explanations for coexistence of multiple fungal species has been29
regulation of resource exchange (Palmer et al., 2003). This mechanism requires that the30
host favours guild members with more beneficial traits, thereby explaining the persistence of31
good mutualists. Such preferential allocation of resources has been documented in the AM32
symbiosis (Kiers et al., 2011; Hammer et al., 2011; Bever et al., 2009; Ji and Bever, 2016)33
and has theoretical support (Bachelot and Lee, 2018; Bever, 2015; Moeller and Neubert,34
2016; Hoeksema and Kummel, 2003; Christian and Bever, 2018; Kˇrivan and Revilla, 2019;35
Valdovinos et al., 2013). However, experimental studies have yielded inconsistent results36
(Fitter, 2006; Kiers and Van Der Heijden, 2006; Walder and van der Heijden, 2015) and no37
physiological basis for host discrimination has been identified. In addition, those experiments38
showing preferential allocation by the plant (allocation of plant carbon to fungi in proportion39
to the benefit received from each fungus) relied on an artificial spatial structure where the40
fungi were spatially segregated (Kiers et al., 2011; Bever et al., 2009; Walder et al., 2012).41
We propose an alternative mechanism that stabilises coexistence of multiple AM fungi42
sharing a single host. We develop a mathematical model to show that asymmetric biomass-43
dependent resource exchange can lead to stable coexistence of multiple AM fungal species,44
without appealing to niche-based mechanisms, spatial segregation, or preferential allocation.45
In our model, carbon transfer depends on plant and fungal biomass, while phosphorus transfer46
depends on both plant and fungal biomass when the plant is small, and effectively on fungal47
biomass only when the plant is large. We show that this asymmetry in nutrient exchange48
results in indirect parasitism between fungal mutualists, where less mutualistic members indi-49
2

rectly parasitise more mutualistic members. These results provide a new perspective on how50
diversity within a guild of mutualists could be maintained.51
Model and Methods52
Formulating a model for a multi-species mutualism53
To investigate the dynamics of multi-species mutualisms we develop a model for the inter-
actions between a host plant and its associated fungal mutualists. Resources exchanged are
phosphorus (fungi to plant) and carbon (plant to fungi). Here, the changes in plant and fungal
biomass are related to the amount of resource received, to the amount of resource given, and
to maintenance costs. All of the mutualists coexist on a single plant, i.e., the carbon provided
by the single plant supports the growth of all of the mutualists. The amount of resource
exchanged depends on the plant and fungal biomass. We use ‘plant biomass’ to indicate the
individual below- and above-ground parts. As it is not feasible to define fungal biomass at
an individual scale, we use the term ‘fungal biomass’ to refer to the population biomass of a
fungal species. In our model therefore, this scenario can be represented by a series of differ-
ential equations describing the change over time of plant biomass (p) and of the biomass (m
i
)
of each of the N species of AM fungi (m
1
, m
2
, .., m
N
):
change in
plant biomass
z}|{
dp
dt
= q
hp
phosphorus
from AM fungi
z }| {
X
i
(α
i
m
i
)
p
d + p
q
cp
carbon
to AM fungi
z }| {
X
i
(β
i
m
i
) p +
intrinsic
growth
z}|{
r
p
p
maintenance
cost
z}|{
µ
p
p
n
, (1a)
dm
i
dt
|{z}
change in
fungal biomass
= q
cm
i
β
i
p m
i
| {z }
carbon
from plant
q
hm
i
α
i
p
d + p
m
i
| {z }
phosphorus
to plant
µ
m
i
m
s
i
| {z }
maintenance
cost
, i = 1 .. N . (1b)
A brief description of the parameters used in the model is given in Table 1. Here, we present54
an overview of the main features of the model.55
The first terms on the right sides of Eqs. (1a) and (1b) describe the gain in plant and fungal56
biomass per unit time due to the resource received. The second terms represent the loss in57
biomass per unit time due to resource given. The relationship between the specific functional58
forms chosen for these terms is tied to the biology, and discussed in detail in the following59
section. The last terms for both equations describes the resource required for maintaining the60
existing biomass. The additional term in Eq. (1a), the intrinsic growth term, represents plant61
growth per unit time in the absence of the fungi (Smith et al., 2003). AM fungi are obligate62
mutualists with no saprobic ability and cannot survive in the absence of the host plant, so no63
intrinsic growth term appears in Eq. (1b).64
Fungal species can be differentiated according to four specific traits: the efficiency with65
which carbon and phosphorus are converted into biomass (q
cm
i
and q
hm
i
) (van Aarle and66
Olsson, 2003), the ability to provide phosphorus to the plant (α
i
) (Ravnskov and Jakobsen,67
1995; Drew et al., 2003), the access to host carbon (β
i
) (Pearson and Jakobsen, 1993; Zhu and68
Miller, 2003) or the maintenance cost (µ
m
i
) (Sylvia and Williams, 1992). Consistent with the69
literature, fungal species in the model can be distinguished accordingly to these four traits.70
The literature provides little evidence about how the maintenance costs of plant and71
fungi depend on their respective biomasses (last term in Eqs. (1a) and (1b)). As density72
dependent and non-density dependent population growth are found in nature (Hassell, 1975),73
we investigate the effect of both linear (i.e. n = 1 and s = 1) and nonlinear forms of the74
maintenance cost term (i.e. n > 1 and s > 1).75
3

Quantification of resource exchange76
Nutrient exchange between the host plant and the fungal mutualists occurs inside the plant77
root cells, where the AM fungi build nutrient exchange zones called ‘arbuscules’ (Peterson78
and Guinel, 2000; Wang et al., 2017). It is reasonable to assume that the amount of phospho-79
rus transferred increases with increasing root colonization and with increasing hyphal length80
(Douds et al., 2000; Treseder, 2013; Sawers et al., 2017); More arbuscules means more contact81
locations where nutrients can be exchanged, and longer hyphae in the soil mean greater fungal82
access to soil phosphorus. In the model, we thus assume a linear relationship between fungal83
biomass and phosphorus transfer.84
The percentage of root colonization by a fungal species is typically between 20% and 50%85
of plant roots, reaching 80% at most (Hart and Reader, 2002; Klironomos and Hart, 2002).86
That is, space availability in the roots seems not to be a factor limiting the presence of AM87
fungi. Thus, we assume that the plant limits phosphorus transfer only when plant biomass is88
small, i.e., when less plant availability implies less habitat for the fungus and therefore less89
phosphorus transfer, but not when the plant is big.90
Mathematically, these assumptions lead to the phosphorus transfer term91
Phosphorus transfer m
i
p
d + p
. (2)92
where d is the half-saturation constant. When p d, phosphorus transfer depends linearly on93
fungal and plant biomass, while when p d, phosphorus transfer depends on fungal biomass94
only. Eq. (2) corresponds to the second term of Eq. (1a) and to the first term of Eq. (1b).95
Eq. (2) implies that in the presence of multiple mutualists, each of the mutualists supplies96
to the plant a quantity of phosphorus per unit time that is proportional to its own biomass.97
Note that, in our model, the non-linearity in the phosphorus transfer term (Eq. (2)) is due98
to a limitation that the fungus experiences at low plant biomass, and not a limitation in the99
benefit of mutualism set by the plant (i.e., the benefit is not saturating at large biomass of100
the species giving the benefit, as seen in previous models of mutualistic interactions (Holland101
and DeAngelis, 2010)). Thus, phosphorus transfer is limited by low plant biomass, but is102
independent of plant biomass (i.e., depends only on fungal biomass) when plant biomass is103
large.104
The literature shows that the plant supplies its associated mutualists with a proportion of105
the carbon it synthesizes (Douds et al., 2000; Treseder and Cross, 2006; Graham, 2000). It has106
been shown that carbon transfer from the plant to the AM fungi depends on photosynthetic107
capacity and on the extent of root colonization by AM fungi (Thomson et al., 1990; Vierheilig108
et al., 2002). In the model, we assume a linear relationship between plant biomass and carbon109
fixation. We further assume a linear relationship between carbon fixation and carbon transfer.110
Finally, we assume linear dependence of carbon transfer and fungal biomass. In sum111
Carbon transfer m
i
p , (3)112
as indicated by the first and second terms of Eqs. (1a) and (1b). The choice of the term113
for carbon transfer in Eq. (3) implies that when multiple mutualists are associated with the114
same host, each species is supplied with an amount of host carbon per unit time that its115
proportional to its individual fungal biomass and to the existing plant biomass. The fungi116
do not directly compete for carbon, but each accesses a different proportion of host carbon117
depending on eachfungus’ biomass.118
One can directly observe that the phosphorus and carbon transfer terms (Eqs. (2) and119
(3)) show a different dependence on the biomass of the supplying and receiving species. These120
differences are tied to the biology of the system, as explained above. Resource exchange is121
4

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References
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"Parasitism within mutualist guilds ..." refers background in this paper

  • ...Other observations, however, show that plant growth is higher in the presence of multiple species of AM fungi than in the presence of any of the species separately (Jansa et al. 2008; Alkan et al. 2006; Maherali and Klironomos 2007; Van der Heijden et al. 1998; Gianinazzi et al. 2010)....

    [...]

Journal ArticleDOI
29 Apr 1960-Science
TL;DR: By emphasizing the very aspects that might result in their denial of them were they less plain the authors can keep the principle explicitly present in their minds untit they see if its implications are, or are noty as unpleasant as their subconscious might suppose.
Abstract: because of a belief that it is best to use that wording which is least likely to hide the fact that we still do not comprehend the exact limits of the principle. For the present, I think the 6'threat of clarity\" (3) is a serious one that is best miniInized by using a formulation that is admittedly unclear; thus can we keep in the forefront of our minds the unfinished work before us. The wording given has, I think, another point of superiority in that it seems brutal and dogmatic. By emphasizing the very aspects that might result in our denial of them were they less plain we can keep the principle explicitly present in our minds untit we see if its implications are, or are noty as unpleasant as our subconscious might suppose. The meaning of these somewhat cryptic remarks should be come clear further on iIl the discussion. What does the exclusion principle mean? Itoughly this: that (i) if two noninterbreeding populations \"do the same thing\"-that is, occupy precisely the same ecological niche in Elton's sense (4)-and (ii) if they are \"sympatric\"that is, if they occupy the same geographic territory-and (iii) if population A multiplies even the least bit faster than population B, then ultimately A will completely displace B, which will become extinct. This is the 44weak form' of the principle. A1ways in practice a stronger form is used, based on the removal of the hypothetical character of condition (iii). We do this because we adhere to what may be caIled the axiom of inequality, which states that no two things or processes

3,062 citations


"Parasitism within mutualist guilds ..." refers background in this paper

  • ...Maria M. Martignoni maria.martignonimseya@ubc.ca Extended author information available on the last page of the article. more beneficial mutualists (Palmer et al. 2003; Hardin 1960)....

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Journal ArticleDOI
11 May 2000-Nature
TL;DR: This issue — commonly referred to as the diversity–stability debate — is the subject of this review, which synthesizes historical ideas with recent advances and concludes that declines in diversity should be expected to accelerate the simplification of ecological communities.
Abstract: There exists little doubt that the Earth's biodiversity is declining. The Nature Conservancy, for example, has documented that one-third of the plant and animal species in the United States are now at risk of extinction. The problem is a monumental one, and forces us to consider in depth how we expect ecosystems, which ultimately are our life-support systems, to respond to reductions in diversity. This issue--commonly referred to as the diversity-stability debate--is the subject of this review, which synthesizes historical ideas with recent advances. Both theory and empirical evidence agree that we should expect declines in diversity to accelerate the simplification of ecological communities.

2,744 citations


"Parasitism within mutualist guilds ..." refers background in this paper

  • ...Previous work has proposed that stable coexistence of multiple species sharing a limiting resource can emerge as a consequence of indirect interactions in multitrophic communities (Stanton 2003; McCann 2000)....

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Journal ArticleDOI
18 Aug 1972-Nature
TL;DR: It is suggested that large complex systems which are assembled (connected) at random may be expected to be stable up to a certain critical level of connectance, and then, as this increases, to suddenly become unstable.
Abstract: Gardner and Ashby1 have suggested that large complex systems which are assembled (connected) at random may be expected to be stable up to a certain critical level of connectance, and then, as this increases, to suddenly become unstable. Their conclusions were based on the trend of computer studies of systems with 4, 7 and 10 variables.

2,424 citations


"Parasitism within mutualist guilds ..." refers background in this paper

  • ..., by predation (May 1972; Caswell 1978; Allesina and Levine 2011; Kerr et al. 2002), or it can alter the effect that one species has on another through higher order interactions, e....

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  • ...The presence of a third species may affect the population size of a superior competitor through an interaction chain, e.g., by predation (May 1972; Caswell 1978; Allesina and Levine 2011; Kerr et al. 2002), or it can alter the effect that one species has on another through higher order…...

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Journal ArticleDOI
TL;DR: A greater understanding of how mycorrhizas function in complex natural systems is a prerequisite to managing them in agriculture, forestry, and restoration.
Abstract: A great diversity of plants and fungi engage in mycorrhizal associations. In natural habitats, and in an ecologically meaningful time span, these associations have evolved to improve the fitness of both plant and fungal symbionts. In systems managed by humans, mycorrhizal associations often improve plant productivity, but this is not always the case. Mycorrhizal fungi might be considered to be parasitic on plants when net cost of the symbiosis exceeds net benefits. Parasitism can be developmentally induced, environmentally induced, or possibly genotypically induced. Morphological, phenological, and physiological characteristics of the symbionts influence the functioning of mycorrhizas at an individual scale. Biotic and abiotic factors at the rhizosphere, community, and ecosystem scales further mediate mycorrhizal functioning. Despite the complexity of mycorrhizal associations, it might be possible to construct predictive models of mycorrhizal functioning. These models will need to incorporate variables and parameters that account for differences in plant responses to, and control of, mycorrhizal fungi, and differences in fungal effects on, and responses to, the plant. Developing and testing quantitative models of mycorrhizal functioning in the real world requires creative experimental manipulations and measurements. This work will be facilitated by recent advances in molecular and biochemical techniques. A greater understanding of how mycorrhizas function in complex natural systems is a prerequisite to managing them in agriculture, forestry, and restoration.

1,776 citations


"Parasitism within mutualist guilds ..." refers background in this paper

  • ...example, the nature of the symbiosis may depend on the genotypes of the interacting species or on environmental conditions (Johnson et al. 1997; Lekberg and Koide 2014)....

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  • ...For example, the nature of the symbiosis may depend on the genotypes of the interacting species or on environmental conditions (Johnson et al. 1997; Lekberg and Koide 2014)....

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Frequently Asked Questions (1)
Q1. What are the contributions mentioned in the paper "Parasitism within mutualist guilds explains the maintenance of diversity in multi-species mutualisms" ?

The authors consider here mutualisms where there are multiple species sharing a resource supplied by the same partner. The authors present a mathematical model, applied to the arbuscular mycorrhizal symbiosis, to propose an alternative explanation for this coexistence. The authors show that asymmetric resource exchange between the plant and its fungal guild can lead to indirect parasitic interactions between guild members.