Potential impacts of climate change on interactions among saprotrophic cord-forming fungal mycelia...

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Potential impacts of climate change on interactions amongsaprotrophic cord-forming fungal mycelia and grazing soilinvertebrates

A. Donald A’BEAR*, T. Hefin JONES, Lynne BODDY

Cardiff School of Biosciences, Cardiff University, Sir Martin Evans Building, Museum Avenue, Cardiff CF10 3AX, UK

a r t i c l e i n f o

Article history:

Received 10 September 2012

Revision received 31 January 2013

Accepted 31 January 2013

Available online -

Corresponding editor: Erik Hobbie

Keywords:

Basidiomycete fungi

CO2 feedback

Decomposition

Global warming

Meta-analysis

Nutrient cycling

Soil fauna

* Corresponding author: Tel.: þ44 029 2087 5E-mail address: [email protected]

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a b s t r a c t

Climate change has the potential to alter the activity of, and interactions among, sapro-

trophic fungi and soil invertebrate grazers, with implications for decomposer community

composition, ecosystem regulation and carbon feedback. We reviewed the impacts of

experimentally manipulated temperature, CO2 concentration and soil moisture content on

saprotrophic cord-forming basidiomycete growth and function, and on the abundance of

soil micro-invertebrates (nematodes) and meso-invertebrates (collembola, mites and

enchytraeids). In warmer and wetter conditions, mycelial growth and mycophagous

invertebrate abundance are likely to increase. Grazers may either consume the extra

mycelial biomass or amplify the temperature effect by stimulating fungal growth. Grazing

can stimulate or inhibit decomposition of colonised woody resources and extracellular

enzyme production. Future empirical study should partition saprotrophic fungi from the

general microbial biomass, with particular attention focussed on enzyme activity and

decomposition. Understanding how biotic and abiotic factors interact to regulate sapro-

trophic fungal activity is crucial to strengthen our predictive capacity regarding decom-

position and carbon feedback under climate change.

ª 2013 Elsevier Ltd and The British Mycological Society. All rights reserved.

Introduction magnitude. Although key drivers of ecosystem processes

Organic carbon decomposition by soil biota generates an

annual global release of 60 Pg (1015 g) C to the atmosphere

(almost 10 times that of fossil fuel emissions); this is balanced

by the approximately equal quantity absorbed through pri-

mary production (Lal 2008). Shifts in this balance, mainly due

to changes in ambient climate, have potentially far-reaching

implications for CO2 feedback and atmospheric gaseous

composition. By 2100, atmospheric CO2 concentration is pre-

dicted to reach 540e970 ppm, accompanied by globally dif-

ferential temperature increases in the range 1.1e6.4 �C (IPCC

2007). Precipitation and the frequency of extreme events are

also expected to increase, with less certainty regarding

729.(A.D. A’Bear).ier Ltd and The British M

AD, et al., Potential imgrazing soil inverteb

(Wardle et al. 1998; Bradford et al. 2002), soil microbes and

invertebrates are not explicitly considered in models predict-

ing impacts of climate change on CO2 feedbacks via, for

example, decomposition and soil respiration (Cao &

Woodward 1998; Cox et al. 2000; Wall et al. 2008). This is pri-

marily a consequence of belowground food web complexity,

the general neglect of the significance of soil interactions in

climate feedback predictions, and the dearth of understanding

of the direct and indirect effects of climate change in soil

(Bardgett et al. 2008).

Impacts of projected climatic scenarios on aboveground

communities and trophic interactions (e.g. plants and their

insect herbivores) have been well-studied and thoroughly

ycological Society. All rights reserved.

pacts of climate change on interactions among saprotrophicrates, Fungal Ecology (2013), http://dx.doi.org/10.1016/

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2 A.D. A’Bear et al.

reviewed (e.g. Bezemer & Jones 1998; Bale et al. 2002; Harsch

et al. 2009; Hooper et al. 2012). Although soil biotic activity

exerts a strong influence on the composition, structure and

functioning of aboveground communities (De Deyn et al. 2003;

van der Heijden et al. 2008), relatively little is known about the

impacts of climate change on belowground community

activity and functioning. Any influence on decomposition,

nutrient cycling and soil organic matter (SOM) dynamics will

be of crucial importance in determining ecosystem-level

responses to climate change at both regional and global

scales (Heimann & Reichstein 2008).

Saprotrophic fungi, in particular, are important regulators

of spatial and temporal variation in nutrient availability, SOM

dynamics and the sensitivity of decomposition to abiotic

variables (Yuste et al. 2011). Basidiomycetes dominate primary

decomposition in forest ecosystems (H€attenschwiler et al.

2005), a globally significant terrestrial carbon store (1240 Pg

C; Lal 2005). A major ecological grouping of these fungi form

extensive mycelial cord networks, mainly restricted to the

woodland soilelitter interface, which link organic resources

and conservatively retain and re-allocate nutrients (Boddy

1993, 1999). Decomposition rates are determined by fungal

community composition, ecophysiological relationships with

abiotic variables, and interactions with other biota.

Soil invertebrates exert the strongest influence on

decomposition where fungi are the dominant component of

the microbial community (Wardle et al. 2004). The low C:N

ratios of fungal cords and hyphae relative to plant-derived

organic matter make mycelia an attractive nutritional source

for soil invertebrates (Boddy & Jones 2008). Mycelial develop-

ment and function can be markedly affected by invertebrate

grazers, including nematodes (Dyer et al. 1992; Crowther et al.

2011a), oribatid mites (A’Bear et al. 2010), collembola

(Kampichler et al. 2004; Tordoff et al. 2008), enchytraeids

(Hedlund & Augustsson 1995), millipedes and woodlice

(Crowther et al. 2011b, c). The dynamics of these interactions

depend on the mycelial form and faunal community; cords

may be ingested by macro-invertebrates, whereas individual

hyphae will also be exploited by smaller invertebrates. Stim-

ulation of mycelial growth can result from low intensity

grazing bymicro- andmeso-invertebrates (Hedlund et al. 1991;

Bretherton et al. 2006) but, more commonly, biomass is

reduced, with macro-invertebrates often removing whole

systems (Crowther & A’Bear 2012). Selective feeding on spe-

cific fungi can differentially affect the competitive abilities of

interacting mycelia, influencing community composition

(Newell 1984a, b; Crowther et al. 2011d).

Elevated temperature and high or low water availability

have the potential to affect soil fungi and invertebrates both

directly and indirectly. Given that CO2 concentrations in soil

are, at least, 10-fold higher than in the atmosphere (Lamborg

et al. 1983; Lal 2008), belowground impacts of elevated CO2

are generally assumed to be indirect, mediated by plant

growth, rhizo-deposition and litter chemistry. The chemical

content of wood and leaf litter could be affected by all of the

abiotic variables considered here, with implications for

decomposition activity of cord-forming mycelial systems.

Elevated CO2, in particular, reduces the nitrogen content and

increases the C:N ratio and structural (e.g. lignin) content of

litter (Cotrufo et al. 1994, 1998; Couteaux et al. 1999; Norby et al.

Please cite this article in press as: A’Bear AD, et al., Potential imcord-forming fungal mycelia and grazing soil invertebj.funeco.2013.01.009

2001). These responses reduce resource quality, often slowing

the rate of decomposition, but could promote the dominance

of lignocellulolytic cord-forming basidiomycetes due to their

ability to decompose the structural components. Reduced

quality of litter could further increase the relative palatability

of nutritionally-conservative fungal mycelia to soil inverte-

brates, potentially increasing their influence on fungal-

mediated decomposition. Such direct and indirect climate

change impacts on saprotrophic cord-forming fungi and their

soil invertebrate grazers will influence the interactions

between these organisms and the ecosystem processes they

facilitate.

This review aims to identify: (1) trends in the responses of

saprotrophic cord-forming fungi and soil invertebrate groups

containing mycophagous members to experimentally

manipulated abiotic variables; (2) implications of these

responses for saprotrophic fungusegrazer interactions under

climate change scenarios; and (3) future research priorities in

terms of biotic and abiotic influences on saprotrophic fungal

activity and functioning. The past 20 years has seen a body of

literature emerge on the responses of potentially mycopha-

gous soil micro-invertebrates (nematodes) and meso-

invertebrates (collembola, mites and enchytraeids) to exper-

imental manipulation of temperature, CO2, precipitation and

drought; these data are synthesised using meta-analysis. This

approach cannot be applied to saprotrophic fungi as they have

rarely been partitioned from the rest of the fungal, or even

microbial, biomass in studies on microbial responses to cli-

mate change. Ecophysiological relationships between sapro-

trophic cord-forming basidiomycetes and abiotic variables

(e.g. temperature and water potential) have, however, been

investigated and are considered. Other abiotic factors asso-

ciated with climate change, such as increasing concentrations

of methane (CH4), ozone (O3) and other gaseous pollutants

(e.g. NOx), will undoubtedly affect both fungi and fauna

directly and indirectly, but as yet insufficient information is

available in the literature to provide informative synthesis.

Impacts of climate change on saprotrophic cord-forming mycelia

Climate change effects on plant productivity influence the

composition and activity of soil microbial communities

(Sadowsky & Schortemeyer 1997; Wolters et al. 2000). Elevated

temperature (e.g. Zhang et al. 2005) and CO2 concentration (e.g.

Zak et al. 1993; Kandeler et al. 2008) have been reported to alter

microbial community composition, favouring fungi. The

extent to which this relates to the abundance and activity of

cord-forming saprotrophs remains unclear. Climate-induced

increases in belowground allocation of photosynthetic car-

bon are known to stimulate root colonisation by mycorrhizal

fungi (Klironomos et al. 1997; Olsrud et al. 2010; Fransson 2012),

which could account for the observed fungal dominance.

There do not, however, appear to be any studies that partition

biomass between saprotrophic and ectomycorrhizal myce-

lium. The ability of saprotrophic fungi to retain nutrients and,

in the case of cord-forming fungi, to translocate them to dif-

ferent regions (Boddy 1993), confers a competitive advantage

over other microbes when nitrogen availability is limited by


Fig 1 e Mycelial extension rate (A) and beech (Fagus

sylvatica) wood inoculum mass loss (B) by Phanerochaete

velutina (-), Hypholoma fasciculare (,), Steccherinum

fimbriatum (:), Phallus impudicus (A), Phanerochaete laevis

(B) and Stropharia caerulea (C) in soil microcosms at

5e25 �C. Error bars are omitted for clarity; where points do

not touch there is no overlap in error. Redrawn from

Dowson et al. (1989) and Donnelly & Boddy (1997).

Climate change and funguseinvertebrate interactions 3

increased plant growth and nutrient uptake (Bardgett et al.

1999). This could increase fungal dominance when climate

change stimulates plant productivity. That recent climate

change is affecting fungal activity is evidenced by changes in

fruiting phenology (Gange et al. 2007).

It is the production of lignin- and cellulose-decomposing

extracellular enzymes by saprotrophic fungi that ultimately

advances the breakdown of wood and litter resources

(Val�a�skov�a et al. 2007). The activity of enzymes is stimulated

by warming, and diffusion of substrates and breakdown

products of decomposition through the soil is facilitated by

water films between soil particles. At a global scale, activities

of many of the commonly assayed soil extracellular enzymes,

involved in carbon, nitrogen and phosphorus cycling, are

correlated with mean annual temperature and precipitation

(Sinsabaugh et al. 2008). Interactive impacts of warming and

altered soil moisture on fungal-mediated enzyme activity are

non-additive; elevated temperature can prevent increased

activity under wetting and reduced activity under drying

(A’Bear et al. unpublished).

Elevated temperature and altered patterns of precipitation

have the potential to alter fungal growth, biomass and activ-

ity. Extension rate of mycelial cord-forming basidiomycetes

generally increases as temperature does, up to optima of

about 20e25 �C, but different species display contrasting

sensitivities and patterns of response across a broad temper-

ature range (Fig 1A; Boddy 1983a). For example, when com-

pared with five other cord-formers, Phanerochaete laevis

extended slowest at low temperatures, but was themost rapid

at 20 and 25 �C (Dowson et al. 1989; Donnelly & Boddy 1997). In

contrast, Phallus impudicus and Hypholoma fasciculare were

stimulated to a lesser extent by warming to these temper-

atures (Fig 1A).

Fungal decomposition of wood also increases with tem-

perature up to similar optima (Boddy 1986; A’Bear et al. 2012).

Mycelial extension often correlates with decomposition rates

of colonised wood resources (Bebber et al. 2011), but temper-

ature sensitivity and optima of these functions can differ for a

given species (Dowson et al. 1989; Wells & Boddy 1995). For

example, P. laevis extended rapidly at higher temperatures,

but was one of the slower decomposers of wood, and although

Phanerchaete velutina and H. fasciculare did not display the

greatest growth response to warming, they were among the

most sensitive with respect to wood decomposition (Fig 1).

Given that current ambientmid-summer temperatureswithin

decaying branches, and upper soil and litter layers of Northern

European temperate forests are sub-optimal for mycelial

growth and decay, rarely reaching 20 �C (Boddy 1983b),

warming has the potential to increase the biomass and

activity of saprotrophic cord-forming fungi. This may not,

however, be true closer to the equator.

Both low and high soil water contents can inhibit fungal

growth and activity (Boddy 1986). At low water content, limi-

tation is due to difficulty in obtaining water for cellular pro-

cesses, basidiomycetes usually being unable to grow below

�4 MPa (Boddy 1984). At high water content, limitation occurs

when conditions are not sufficiently aerobic. Elevated tem-

perature can exacerbate the limitation imposed by both low

and high water contents. At already low water content,

physiological stress can be accentuated by warming-induced


soil moisture loss. At high water content, when temperature

is elevated towards the optimum for activity, limitation occurs

because of insufficient capacity for gaseous exchangewith the

atmosphere, due to water filling voids, cannot accommodate

the need for more rapid diffusion of O2 into, and CO2 out of,

soil and organic resources. Increased precipitation generally

promotes fungal activity as long as conditions remain suffi-

ciently aerobic. In naturally wet soils (e.g. bogs and tropical

rainforest), moisture loss could relax anaerobic constraints on

biological processes (Cleveland et al. 2010), increasing sapro-

trophic activity. Studies involving irrigation and drought

manipulations have found fungal biomass and community

composition to be fairly resilient to fluctuating moisture

conditions (Yuste et al. 2011), displaying minimal responses

relative to seasonal variation (Williams & Rice 2007; Hawkes

et al. 2011). Impacts are likely to differ between fungal



groups; responses of saprotrophic fungi have yet to receive

any specific attention with respect to natural or experimental

irrigation and drought.

Cord-forming basidiomycetes show species-specific sen-

sitivity to low soil water potential, but commonly display

increased hyphal aggregation into cords (Dowson et al. 1989;

Donnelly & Boddy 1997; Wells et al. 2001), which are more

desiccation-resistant than non-cording hyphae. Water

potential optima for mycelial extension and biomass pro-

duction in soil tend to lie between �0.01 and �0.02 MPa,

whereas decay optima are often lower, but generally not

below �0.1 MPa (Dowson et al. 1989; Donnelly & Boddy 1997).

Like other basidiomycetes, in agar culture cord-forming sap-

rotrophs cannot growmuch below�4.4MPa,many being even

more sensitive (Boddy 1983a; 1984). Water can, however, be

translocated through cords, allowing them potentially to grow

from moist to drier regions, the dry rot fungus of buildings,

Serpula lacrimans, being a classic example (Cairney 1992). Cord-

forming fungi might also alter their growth location under

different climatic scenarios. For example, in UK temperate

forests extensive cord systems of Megacollybia platyphylla

develop at the soilelitter interface, whereas in the drier soils

of Massachusetts they develop 5e10 cm below the surface

litter (L Boddy pers. obs.). In addition to effects on growth,

lowering of water potential also affects carbon utilisation and

nutrient translocation. When new woody resources were

added to cord systems in soil microcosms, colonisation had a

significant carbon (energy) cost compared to controls, and

phosphorous acquisition was reduced (Wells et al. 2001). Rel-

atively minor fluctuations in soil moisture content are

unlikely to prevent an increase in saprotrophic mycelial bio-

mass and activity under elevated temperature and CO2. Less

predictable extremes, such as prolonged periods of drought or

precipitation, will have a more pronounced influence.

Climate change has the potential to alter the composition

of saprotrophic cord-former communities by differentially

influencing the growth and activity of individual mycelial

systems, and altering the outcome of interspecific inter-

actions. Competition between mycelial systems is a major

driver of fungal distribution and community development,

both in organic substrata and in soil (Boddy 2000). When small

mycelial systems of cord-forming basidiomycetes encounter

each other in soil, a stronger combatant replaces a weaker one

and becomes the main regulator of decomposition in a given

area of forest floor (Dowson et al. 1988a, b). During interspecific

mycelial interactions, enzyme production and nutrient loss

from mycelia increase markedly (Wells & Boddy 2002; �Snajdr

et al. 2011).

Abiotic factors, such as temperature, water potential and

gaseous regime, affect the rate of progression and outcome of

interactions (Boddy et al. 1985; Griffith & Boddy 1991; Boddy

2000). For example, in agar culture, H. fasciculare does not

replace Phlebia radiata at 20 �C but it does at 25 �C. Differential

sensitivity to temperature (Fig 1A) can either accelerate the

progression of the dominant competitor through its oppo-

nent’s mycelium, or reverse the outcome of the interaction by

stimulating combative activity of the weaker competitor to

the extent that it becomes dominant (Schoeman et al. 1996;

Crowther et al. 2012b). Competitive abilities of individual

species tend to diminish towards the lower end of their water


potential (Boddy 2000) and upper end of their CO2 tolerance

range (Chapela et al. 1988). Interspecific variation in the sen-

sitivity of cord-forming basidiomycetes to climatic variables

could, therefore, drive shifts in community structure and

functioning. Species-specific extracellular enzyme production

and fungal-mediated decay rates suggest that community

composition will have a strong influence on decomposition.

Impacts of climate change on soil invertebrates

Meta-analysis

Data were collected from published studies reporting the

effects of elevated temperature, CO2 and precipitation, and

drought on groups of soil micro- and meso-invertebrates

containing mycophagous members: nematodes (phylum

Nematoda), mites (subclass Acari), collembola (subclass Col-

lembola) and enchytraeids (family Enchytraeidae). There are

currently insufficient empirical data available on the respon-

ses of mycophagous macro-invertebrate groups to climatic

manipulation to make meta-analysis informative. Studies

were identified by searching ISI Web of Knowledge databases,

personal reference collections and literature cited therein.

Measurements were related to abundance (e.g. population

density, number g�1 dry soil). Control and treatment means,

errors and replication (n) were recorded for each measure-

ment. In the source studies, elevated temperatures varied

from 1.5 to 5 �C above summer ambient, elevated CO2 from 200

to 350 ppmabove ambient, and increased precipitation (where

defined) from 10 to 40% permonth above ambient. Therewere

sufficient data to analyse the responses of nematodes, mites,

collembola and enchytraeids to a range of climatic manipu-

lations. Nematode feeding biology is well documented (e.g.

Yeates et al. 1993), enabling responses of bacterial, fungal,

plant and carnivorous feeding guilds to be considered sepa-

rately within this taxon.

The natural logarithm of the response ratio (lnR) was used

as the effect size metric to reflect relative changes in soil

invertebrate abundance:

lnR ¼ lnðXT=XCÞ;where XT and XC are the mean abundance of the treatment

and control groups, respectively. The logarithm linearises the

metric so that deviations in the numerator are treated in the

same way as deviations in the denominator; this normalises

the distribution (Hedges et al. 1999). Positive values indicate an

increase in the response variable with respect to the climatic

factor. The mean, variance and bootstrapped 95 % confidence

intervals of lnR were calculated in MetaWin 2.1 (Rosenberg

et al. 2000) with n as the weighting function.

Responses to climate manipulations

Meta-analysis of data from published studies revealed that

climate change impacts on soil invertebrate abundance vary

according to climatic treatment, taxonomic group and in the

case of nematodes, feeding guild (Fig 2). The lack of an effect of

elevated temperature on collembola and mite abundance

could appear counter-intuitive, until the close relationship


Fig 2 e Meta-analysis of published studies reporting

climate change impacts on soil invertebrate populations.

Effect sizes (lnR [[ln(XE/XC), where XE and XC are mean

abundance of the treatment and control groups,

respectively] ± bootstrapped 95 % CI) resulting from soil

invertebrate abundance responses to elevated temperature

(T), elevated CO2, increased precipitation (P) and drought

(D). Effects are significant (P < 0.05) where CIs do not

overlap zero. Climatic factors and the number of



between temperature and soil moisture is considered.

Warming-induced moisture loss at the soilelitter interface,

rather than a direct physiological response to temperature, is

the most likely factor limiting population growth due to the

desiccation sensitivity of soil invertebrates (Convey et al. 2002;

Dollery et al. 2006; Day et al. 2009). Enchytraeids increased in

abundance at elevated temperature (Fig 2); they avoid adverse

moisture conditions by migrating downwards within the soil

profile (Maraldo et al. 2008). The influence of temperature on

enchytraeid reproduction rate (Briones et al. 1997) often

stimulates population growth deeper in the soil profile, or in

naturally wet soils (e.g. peatlands; Briones et al. 2004; Carrera

et al. 2009). Nematodes were not affected by temperature

overall, but feeding guilds displayed differential responses;

plant-feeders decreased, whereas fungivores and carnivores

increased in abundance (Fig 2).

As moisture is a common limiting factor for soil inverte-

brate abundance and diversity (Briones et al. 1997; Lindberg

et al. 2002), increased wetting and drying of the soil environ-

ment could potentially be one of the most important climate

change factors in terms of direct effects on soil invertebrate

communities. The moisture limitation imposed by drought

reduced the abundance of collembola, mites, enchytraeids,

and plant- and bacterial-feeding nematodes (Fig 2). Enchy-

traeids and free-living nematodes are highly dependent on

free water in soil for motility and survival (Briones et al. 1997;

Kardol et al. 2010). Precipitation regimes will have significant

impacts on responses to other climatic factors, particularly

elevated temperature. Increased precipitation alone only

increased nematode abundance, but, in combination with

elevated temperature, also increased the abundance of col-

lembola and mites (Fig 2). Warming accentuated the negative

effect of drought on mites (Fig 2).

Elevated CO2 reduced the abundance of mites (95 % CI just

overlapping zero) and nematodes (except plant-feeders)

(Fig 2). The collembola, mites and enchytraeids that graze on

fungi also contribute to litter transformation, providing a

potential pathway for effects independent of the fungal food-

chain. Decreased nitrogen and increased tannin concen-

trations in leaf litter grown under elevated CO2 (Lindroth et al.

1995; King et al. 2001) are known to reduce the abundance of

litter transformers (Loranger et al. 2004; Meehan et al. 2010). By

reducing plant transpiration, elevated CO2 can alleviate

temperature-inducedmoisture loss from soil (Field et al. 1995),

potentially explaining the positive interactive effect of

warming and CO2 on collembola and mites (Fig 2).

The role of soil invertebrates in decomposition is greatest

where temperature and moisture constraints on biological

activity are relaxed (Wall et al. 2008), increasing their abun-

dance, as shown by the interactive positive effect of elevated

temperature with CO2, precipitation or both on all analysed

taxa (Fig 2). Regions becoming warmer and wetter due to cli-

mate change could experience accelerated decomposition

rates as the abundance of soil invertebrates and their role in

this process increase. It is less clear how indirect impacts of

soil fauna on decomposition, mediated by interactions with

observations are indicated for each effect size. Sources are

provided in the Supplementary information (Table S1).



the heterotrophic microbial community, will alter if their

abundance and community composition change as predicted.

Implications for saprotrophicfunguseinvertebrate interactions

Trophic interactionswithin the decomposer community, such

as those between saprotrophic fungi and their invertebrate

grazers, are crucial in determining ecosystemeatmosphere

carbon feedbacks under climate change (Fig 3). Abiotic con-

ditions that stimulate saprotrophic fungal biomass pro-

duction and activity are also likely to increase soil invertebrate

abundance. As well as being influenced directly (temper-

atureemoisture characteristics of soil) and indirectly (medi-

ated by primary production) by climate change, fungi and

invertebrates are affected by interactions with each other

(Fig. 3). Mycophagous soil invertebrates have the potential to

drive, and respond to, changes in fungal community compo-

sition (Klironomos et al. 1992, 1997; Jones et al. 1998).

Temperate regions are generally predicted to become

warmer and wetter as a consequence of climate change (IPCC

Fig 3 e Conceptual model of the impacts of climate change

on interactions between saprotrophic cord-forming

basidiomycetes and their soil invertebrate grazers in

woodland ecosystems, and direct (closed arrows) and

indirect (dashed arrows) feedback routes to CO2

production, via decomposition. Direct effects include the

influence of temperature and altered precipitation on the

abundance and activity of these organisms, whereas

indirect effects are mediated by climate-driven changes in

plant productivity, influencing soil physiochemical

properties and interactions between saprotrophic mycelia

and with invertebrate grazers.


2007), potentially increasing saprotrophic mycelial biomass

and invertebrate grazer abundance. Decomposition rates are

determined, in part, by the balance between extra-resource

mycelial growth (energetic exploitation of the resource, lead-

ing to the colonisation of new ones) and removal by grazing

invertebrates. The direct stimulation of mycelial growth and

activity due to climate change could be indirectly influenced

by increased grazer abundance, with implications for the rate

at which new resources are encountered and subsequently

decomposed (Fig 3).

Few studies have attempted to advance mechanistic

understanding of the consequences for primary decom-

position resulting from concurrent climate-induced stim-

ulation of mycelial growth and invertebrate grazer

abundance. In a microcosm experiment investigating the

effect of elevated temperature on the foraging and decom-

position of beech (Fagus sylvatica) wood by five saprotrophic

basidiomycetes, in factorial combinations with two mycoph-

agous collembola species, grazing mediated the responses of

fungal growth and functioning to warming (A’Bear et al. 2012).

Collembola abundance, and therefore, grazing pressure

increased at elevated temperature, but only when feeding on

particular fungi. Increased grazing pressure can counteract, or

even amplify, warming-induced stimulation of mycelial

growth. Accelerated radial extension of Resinicium bicolor and

P. impudicus at elevated temperature was prevented by

increased abundance of Folsomia candida and Protophorura

armata (Collembola), respectively, whereas F. candida ampli-

fied the stimulatory effect of warming on H. fasciculare (Fig 4).

In more realistic systems, where collembola are not

restricted to a single resource, the bottom-up influence on

their abundance could be less pronounced. In woodland soil

mesocosms, however, inoculation with cord-forming basi-

diomycetes limits the size, and ability to respond to climate

manipulation, of mycophagous collembola populations

(A’Bear et al. unpublished). The mechanism behind this con-

straint is thought to reflect resource-limitation imposed by the

competitive suppression of the more palatable fine hyphae of

soil microfungi by thick cords. Removal of cords by woodlice,

with their larger body size and greater metabolic require-

ments, could prevent the exclusion of less competitive fungi

and remove this limitation on collembola population size

(Crowther et al. 2012a).

Removal of mycelia by high intensity grazing stimulates

wood decomposition by H. fasciculare and R. bicolor, even

though there is less extra-resource fungal biomass to support,

as the fungus utilises more resource-derived energy to

maintain explorative growth (Crowther et al. 2011a). Extrac-

ellular enzyme production (involved in carbon, nitrogen and

phosphorus cycling) by mycelial systems is also influenced by

grazing. Fungi display differential enzymatic responses to

grazing; production by R. bicolor is reduced, and that by H.

fasciculare and Phanerochaete velutina increased, with grazer-

specific impacts on different enzymes (Crowther et al. 2011c).

Increased soil invertebrate abundance could stimulate both

extracellular enzyme production and primary decomposition

by basidiomycete mycelia, though this has not yet been

investigated.

Mycophagous woodlice and millipedes typically have

stronger effects on mycelial growth (Crowther et al. 2011a;


Fig 4 e Mycelial extension rate (±SEM) of Hypholoma

fasciculare (A), Phallus impudicus (B) and Resinicium bicolor

(C) in soil microcosms at ambient (15 �C based on late

summer e autumn temperatures beneath the litter layer in

UK temperate woodland (Boddy 1983b); TA, open bars) and

elevated (ambient D 3 �C; TE, shaded bars) temperature in

un-grazed, Folsomia candida-grazed and Protophorura

armata-grazed systems. Significant (*P < 0.05; **P < 0.01)

differences in extension between ambient and elevated

temperature are indicated for different grazing treatments

(one-way ANCOVA). Redrawn from A’Bear et al. (2012).


Crowther & A’Bear 2012) and extracellular enzyme production

(Crowther et al. 2011d) than micro- and meso-invertebrates.

Relatively few studies have investigated species and pop-

ulation level responses of macro-invertebrates to climate

change (e.g. Zimmer 2004; David & Gillon 2009); warming is


expected to stimulate population growth rates of some tem-

perate woodlouse and millipede species, increasing their

abundance and influence on decomposition (reviewed by

David & Handa 2010).

Selective grazing on specific fungi has the potential to

influence community composition by differentially affecting

the competitive abilities of interacting mycelia. By preferen-

tially consuming the stronger competitor, collembola can

increase the relative abundance of a weaker, but less palat-

able, species (Newell 1984a, b). Via the same mechanism, the

stronger impact of woodlouse grazing can result in the com-

plete replacement of the dominant fungus by an inferior

competitor (Crowther et al. 2011d). In contrast, growth stim-

ulation of the weaker species by low-intensity nematode

grazing can also reverse the interaction outcome. There is

potential for climate-driven changes in soil invertebrate

abundance to influence the direct impact of abiotic factors on

competitive interactions. Elevated temperature stimulated R.

bicolor growth, enabling it to out-compete the formerly dom-

inant P. velutina (Crowther et al. 2012b). The concurrent

increase in grazing pressure on R. bicolor, however, counter-

acted the impact of warming on the interaction outcome.

Patchy and aggregative distributions of invertebrates in nat-

ural systems will exert unequal grazing pressures on com-

peting fungi. Woodlice limited to the territory of one

competing mycelium can prevent the dominance of any one

species and, indirectly, moderate the influence of warming

where interaction outcomes were reversed in the absence of

grazing (A’Bear et al. in press). The consequence of shifting

mycelial dominance for decomposition rates requires further

investigation using longer-term experiments. Interactions

between biotic and abiotic factors will regulate decomposer

community composition and function of saprotrophic cord-

forming fungi under climate change.

Conclusions

Climate change predictions for a warmer and wetter envi-

ronment are likely to stimulate the activity of saprotrophic

cord-forming basidiomycetes and increase the abundance of

mycophagous soil invertebrates. Althoughwarming-induced

increases in mycelial growth could, to some extent, be

counteracted by grazing, there is potential for increased

production and release of extracellular enzymes into the soil

environment, and accelerated primary decomposition of

colonised resources. To improve our mechanistic under-

standing of climate change impacts on decomposition, sap-

rotrophic fungal activity needs to be partitioned from that of

the general microbial biomass in empirical investigations.

The majority of studies published to date have not done this,

making functional implications of the overall trends difficult

to identify. Future research should consider interactive

effects of climate change factors on soil biota, particularly

given the influence of elevated temperature and CO2 on soil

moisture properties. Understanding how biotic and abiotic

factors interact tomediate saprotrophic fungal functioning is

crucial in enhancing our predictive capabilities regarding

primary decomposition and carbon feedback in a changing

climate.



Acknowledgements

Two anonymous reviewers made thoughtful suggestions to

improve the manuscript. Natural Environment Research

Council for provision of a studentship to ADA (NERC/I527861).

Supplementary data

Supplementary data related to this article can be found at

http://dx.doi.org/10.1016/j.funeco.2013.01.009.

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