Biol. Rev. (2016), pp. 000–000.

1
doi: 10.1111/brv.12305

How lichens impact on terrestrial community

and ecosystem properties
Johan Asplund1,∗ and David A. Wardle2
1
Department of Ecology and Natural Resource Management, Norwegian University of Life Sciences, PO Box 5003, NO-1432 Ås, Norway
2
Department of Forest Ecology and Management, Swedish University of Agricultural Sciences, SE-901 83 Umeå, Sweden

ABSTRACT

Lichens occur in most terrestrial ecosystems; they are often present as minor contributors, but in some forests, drylands
and tundras they can make up most of the ground layer biomass. As such, lichens dominate approximately 8% of
the Earth’s land surface. Despite their potential importance in driving ecosystem biogeochemistry, the influence of
lichens on community processes and ecosystem functioning have attracted relatively little attention. Here, we review
the role of lichens in terrestrial ecosystems and draw attention to the important, but often overlooked role of lichens
as determinants of ecological processes. We start by assessing characteristics that vary among lichens and that may
be important in determining their ecological role; these include their growth form, the types of photobionts that they
contain, their key functional traits, their water-holding capacity, their colour, and the levels of secondary compounds in
their thalli. We then assess how these differences among lichens influence their impacts on ecosystem and community
processes. As such, we consider the consequences of these differences for determining the impacts of lichens on
ecosystem nutrient inputs and fluxes, on the loss of mass and nutrients during lichen thallus decomposition, and on
the role of lichenivorous invertebrates in moderating decomposition. We then consider how differences among lichens
impact on their interactions with consumer organisms that utilize lichen thalli, and that range in size from microfauna
(for which the primary role of lichens is habitat provision) to large mammals (for which lichens are primarily a food
source). We then address how differences among lichens impact on plants, through for example increasing nutrient
inputs and availability during primary succession, and serving as a filter for plant seedling establishment. Finally we
identify areas in need of further work for better understanding the role of lichens in terrestrial ecosystems. These
include understanding how the high intraspecific trait variation that characterizes many lichens impacts on community
assembly processes and ecosystem functioning, how multiple species mixtures of lichens affect the key community-
and ecosystem-level processes that they drive, the extent to which lichens in early succession influence vascular plant
succession and ecosystem development in the longer term, and how global change drivers may impact on ecosystem
functioning through altering the functional composition of lichen communities.

Key words: decomposition, functional traits, invertebrate food webs, lichenized fungi, nutrient cycling, trophic
interactions.

CONTENTS
I. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2
II. Characterizing the diversity of lichen growth forms and functional characteristics . . . . . . . . . . . . . . . . . . . . . . . 2
(1) Growth forms . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3
(2) Associations with photobionts . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4
(3) Functional traits . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4
(4) Moisture characteristics . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5
(5) Pigmentation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6
(6) Carbon-based secondary compounds . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6

* Address for correspondence (Tel: +47 6723 1654; E-mail: johan.asplund@nmbu.no)

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2 Johan Asplund and David A. Wardle

III. How variation among lichens affects ecosystem nutrient and carbon flux . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6
(1) Biogeochemical nutrient cycling . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6
(2) Litter decomposition . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7
IV. How variation among lichens affects their interactions with consumers . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8
(1) Lichen food webs . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8
(2) Defence . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11
V. How variation among lichens affects their impacts on soils and plants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12
VI. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 13
VII. Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 14
VIII. References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 14

I. INTRODUCTION functional traits may have a more important direct role than
macroclimate in driving ecosystem processes (Cornwell et al.,
Lichens are symbiotic associations between a heterotrophic 2008). This has led to calls for a shift from species-centred
mycobiont (i.e. fungus) and one or more autotrophic to trait-centred approaches in understanding community
photobionts (green algae and/or cyanobacteria). Lichens and ecosystem processes (McGill et al., 2006; Violle & Jiang,
are generally slow-growing, long-lived and stress-tolerant, 2009). However, the importance of functional traits for
but they show a wide diversity of growth forms (Fig. 1). driving ecological processes in other ecologically important
As such, some are prostrate and have leaf-like structures, autotrophs such as lichens has seldom been acknowledged
while others have complex three-dimensional structures that (e.g. Lang et al., 2009; Asplund & Wardle, 2013; Zedda &
resemble minute forests. Lichens occur in most terrestrial Rambold, 2015). Despite this, lichens have a distinct suite of
ecosystems; often they occur as minor contributors, but in functional traits that are analogous to the types of functional
some forest, grassland and tundra ecosystems they make up a traits frequently studied for vascular plants (Cornelissen et al.,
large proportion of the ground-layer biomass. Further, they 2007), and that potentially provide a mechanistic framework
frequently dominate in habitats that are too nutrient-poor, for understanding their contribution to community and
too dry, or too cold to support a complete or permanent ecosystem processes.
cover of plants. As such, lichens dominate approximately 8% Herein we review the role of lichens in terrestrial commu-
of the Earth’s land surface (Nash, 2008), and most of the land nities and ecosystems. We start by discussing the functional
surface in xeric high-latitude and high-elevation ecosystems. characteristics of lichens, with particular focus on their traits
More than 18000 species of lichens exist worldwide and at and functional groupings because of their potential impor-
higher latitudes the number of lichen species exceeds the tance in driving lichen species effects on community and
number of vascular plant species (Nash, 2008). ecosystem processes. We then explore the role that variation
Most literature about how autotrophs affect ecosystem among lichens has in determining ecosystem carbon (C) and
processes has focused on vascular plants, and over the past nutrient fluxes, for instance by affecting the decomposition
25 years an enormous literature has emerged on how plant and nutrient loss from their residues. Following that, we
species differences drive ecosystems (Hobbie, 1992; Grime, discuss how differences among lichens in their structural
2001; Wardle, 2002). As such, it is well recognized that and functional characteristics affect their interactions with
vascular plant species identity influences biogeochemical animals and plants, and the ecological consequences of
processes through determining the quantity and quality these effects. By addressing these topics in combination
of litter that enters the soil, and inputs of nitrogen (N) we draw attention to the important but often overlooked
through biological N2 fixation. By contrast, despite their role of lichens as community and ecosystem drivers, and
importance in many ecosystems worldwide, the influence of identify areas which are in need of further work for better
lichens on community processes and ecosystem functioning understanding the role of lichens in terrestrial ecosystems.
has attracted less attention and is often overlooked. This
is despite their potential importance in driving ecosystem
biogeochemistry. As such, most lichen species capture nutri-
ents from the air and roughly 10% of them fix atmospheric II. CHARACTERIZING THE DIVERSITY OF
N2 through their association with cyanobacteria. These LICHEN GROWTH FORMS AND FUNCTIONAL
nutrients trapped by lichens reach other ecosystem compo- CHARACTERISTICS
nents through leaching, decomposition and consumption by
animals. Further, lichens also provide habitats for various How lichens drive communities and ecosystems is regulated
invertebrates that may or may not use them as a food source. by a number of ways in which lichens differ. These include
Many studies on vascular plants have shown that the their growth form, associations with symbionts, thallus
effect of species on ecosystem processes depends on their nutrient concentrations, specific thallus mass (STM; the
functional traits (Cornelissen et al., 1999; Díaz et al., 2004; equivalent of a plant’s specific leaf mass or the reciprocal of
Kurokawa, Peltzer & Wardle, 2010), and that variation in specific leaf area), capacity for water retention, colour and

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How lichens impact on communities and ecosystems 3

Fig. 1. Lichens show tremendous variation both in terms of their growth form and colour. Upper three panels (left to right) are
the crustose lichens Caloplaca epithallina, Carbonea vitellinaria and Icmadophila ericetorum. The middle panels (left to right) are the foliose
lichens Lobaria pulmonaria, Arctoparmelia centrifuga and Leptogium saturninum. The lower three panels (left to right) are the fruticose lichens
Cladonia stellaris, Ramalina calicaris and Bryoria nitidula. Photos are © Einar Timdal.

secondary compounds (Fig. 2). Below, we explore each of penetration and expansion/contraction of lichen thalli) and
these characteristics in turn. chemical processes (via excretion of various organic acids)
(Chen, Blume & Beyer, 2000). Furthermore, many crustose
lichens are grazed by invertebrates (Baur, Fröberg & Baur,
(1) Growth forms 1995). Meanwhile foliose (i.e. leaf-like) lichens are loosely or
Lichenized fungi form vegetative structures that are much tightly attached to their substrate. The lobes of these lichens
more complex than those of most other fungi. There is a great sometimes overlap like tiles, and the lower side often has
variability in the physical structure of lichens and they are a tomentum or anchoring rhizinae, which helps generate
traditionally divided into three main morphological groups: favourable microclimate and microhabitat conditions for
crustose, foliose and fruticose. However, there is a high level different invertebrates. Fruticose lichens always stand out
of morphological diversity within these groups which results from the surface of their substrate. These are hair-like,
in contrasting functional characteristics. Crustose lichens are strap-shaped or shrubby, with considerable variation in
tightly adhered to their substrate (often tree bark or rock, branching pattern. Their size varies from minute species
but sometimes evergreen tree leaves in moist forests) from of 1–2 mm to species up to 3 m long (Brodo, Sharnoff &
which they cannot be removed without destruction. Some Sharnoff, 2001). An extreme growth form of these fruticose
are very thin and do not produce much biomass, suggesting lichens includes vagrant epiphytic lichens that lack holdfasts
that their direct role in biogeochemical cycling probably is in mature specimens, and that occupy the air spaces between
limited. However, other crustose lichens, particularly those branches of trees. Such lichens (e.g. Usnea longissima) can be
that are endolithic (i.e. growing inside rocks), may induce >1 m long and their hair-like tissues tend to degrade when
rock weathering through both physical processes (via hyphal in direct contact with the tree branch (Gauslaa, 1997).

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4 Johan Asplund and David A. Wardle

[Property of Lichen] [Ecological consequence]

Nutrient status
Growth form Decomposition
Shelter for invertebrates
Invertebrate community assembly
Structural complexity
Rainfall and nutrient interception
Water uptake and retention
Crustose Foliose Fruticose

Nutrient accumulation
N2-fixation
Plant growth
Photobiont Nutrient status
Consumption by invertebrates
Water uptake and retention
Rainfall and nutrient interception

Green algae Cyanobacteria Green algae +

Cyanobacteria

Decomposition
Nutrient status
Functional traits Consumption by invertebrates
Water uptake and retention
Rainfall and nutrient interception

Resource conservative Resource acquisitive

Nutrient status Decomposition

Water-holding capacity
(WHC) Water uptake and retention Consumption by invertebrates
Soil moisture Rainfall and nutrient interception

Low WHC High WHC

Microbial abundance and activity

Soil/substrate temperature
Colour Decomposition
Albedo
Rock weathering

Light Dark
O
O O
O
O O
Decomposition
O O
Consumption by invertebrates
Secondary compounds O O Defence of thallus tissue
O
O
O Microbial abundance and activity
OH
O O Rock weathering
Strong defence Weak defence

Fig. 2. Lichens vary greatly in terms of growth form, type of photobiont, functional traits, water-holding capacity, colour and
secondary chemistry. This variation results in species-specific differences in the effect lichens have on community and ecosystem
properties. Photos are © Einar Timdal.

(2) Associations with photobionts below overhanging rocks or on the leeside parts of lower old
spruce trunks (Smith et al., 2009). Meanwhile, cyanolichens
In addition to their growth form, lichenized fungi also vary
need liquid water to activate photosynthesis (Lange et al.,
in their associations with their photobionts, and this can have
1986), which explains why they are most abundant in
important ecosystem-level implications. Chlorolichens have
rainforests and open sites with frequent heavy dewfall
green algae as their only photobiont, whereas cyanolichens
(Gauslaa, 2014).
have cyanobateria as their only photobiont, while
cephalolichens have green algae as their main photobiont but
also contain cyanobacteria in localized internal or external (3) Functional traits
structures (i.e. cephalodia). The most obvious difference Lichens have a high diversity of functional traits associated
between these groups is that those lichens which contain with resource uptake and retention (Cornelissen et al., 2007;
cyanobacterial symbionts commonly fix N2 and thus have Asplund & Wardle, 2013), which may potentially play an
a higher N concentration. However, these groups also important role in determining their effects on ecological
differ in their water relations, which in turn influence processes (Lang et al., 2009) and associated invertebrate
both their physical structure and water-holding capacity. communities (Bokhorst et al., 2015). These traits include
As such, chlorolichens and cephalolichens readily activate thallus nutrient concentration, defence compounds, STM
their photosynthesis in equilibrium with high ambient air and water-holding capacity, and are analogous to vascular
humidity (Lange, Kilian & Ziegler, 1986), and some of them plant leaf functional traits that are widely recognized as
even prefer habitats that are deficient in liquid water such as important ecological drivers (Table 1). However, very few

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How lichens impact on communities and ecosystems 5

Table 1. Range of trait values (2.5 and 97.5% quantiles) observed globally for a range of functional traits, for vascular plants (from
the TRY database; Kattge et al., 2011) and lichens (data from Demmig-Adams et al., 1990; Gauslaa & Solhaug, 1998; Smith &
Griffiths, 1998; Palmqvist et al., 2002; Lange et al., 2004; Gauslaa, 2005; Nybakken, Johansson & Palmqvist, 2009; Solhaug et al.,
2009; Nybakken et al., 2010; Gauslaa & Coxson, 2011; Nybakken, Sandvik & Klanderud, 2011; Raggio et al., 2012; Asplund &
Wardle, 2013, 2014; Esseen et al., 2015; Asplund, Ohlson & Gauslaa, 2015b; Gauslaa et al., 2016)

2.5% 97.5% Equivalent 2.5% 97.5%

Plant trait N quantile Median quantile lichen trait N quantile Median quantile
Leaf tissue N (%) 33880 0.8 1.7 3.9 Tissue N (%) 98 0.3 1.3 4.5
Leaf tissue P (%) 17057 0.04 0.13 0.35 Tissue P (%) 34 0.02 0.11 0.31
Leaf tissue C (%) 7856 40.5 47.6 54.1 Tissue C (%) 21 37.6 44.7 49.0
Specific leaf mass 45733 2.1 5.7 22.2 Specific thallus 54 6.4 12.3 40.3
(mg m−2 ; mass (STM;
reciprocal of mg cm−2 )
specific leaf area)
Phenolic 454 2.4 11.9 25.1 Phenolic 28 0 2.7 23.7
compounds (%) compounds (%)
Leaf dry matter 16185 0.1 0.2 0.4 Water holding 27 5.4 12.9 60.2
content (LDMC; capacity (WHC;
g g−1 ) mg H2 O cm−2 )∗
Maximum 2384 0.02 0.12 0.49 Maximum 58 0.002 0.014 0.042
photosynthetic photosynthetic
rate per leaf dry rate per thallus
mass (Amax ; dry mass
μmol g−1 s−1 ) (μmol g−1 s−1 )
∗
Lichens are poikilohydric and their water content is heavily dependent on water availability (liquid or air humidity). As such, LDMC and
WHC are not functionally analagous. The maximum water holding capacity is highly variable and mostly driven by STM and growth
form, and WHC within species are strongly related to thallus size (Gauslaa & Solhaug, 1998).

studies have sought to characterize the variation of lichen & Green, 1981; Gauslaa et al., 2009; Solhaug et al., 2009;
functional traits that occurs in natural communities, or Asplund, Sandling & Wardle, 2012).
whether lichens show trade-offs in traits between those
that are characteristic of rapid resource acquisition versus (4) Moisture characteristics
resource conservation in the manner frequently shown for
vascular plants (Grime et al., 1997; Díaz et al., 2004; Wright Lichens vary greatly in their ability to retain moisture, and
et al., 2004). Recently, it has been shown that within-species this has important ecological implications. Some lichens (e.g.
variation in lichen functional traits can be more important those that are thin and pendulous) generally have a limited
than variation across species (and thus species turnover) in ability to retain water (Esseen et al., 2015), even though they
determining community-weighted trait variation across a quickly take up water from humid air. Meanwhile, some
strong environmental gradient (Asplund & Wardle, 2014). other lichens (typically thick or gel-like foliose cyanobacterial
This contrasts with what is usually found for vascular plants lichens) have the ability to retain water for lengthy periods
where across-species variation in species turnover is usually (Lange et al., 1993; Gauslaa & Solhaug, 1998; Lange, Belnap
more important (Kichenin et al., 2013; Siefert et al., 2015). & Reichenberger, 1998; Lange, 2000). The water-holding
However, other than the work of Asplund & Wardle (2014), capacity of lichens is strongly positively correlated with
no study has attempted to disentangle species turnover from their STM both within and across species (Gauslaa &
within-species trait variability effects for lichens and more Coxson, 2011; Merinero, Hilmo & Gauslaa, 2014; Esseen
studies are needed to see if the outcome that they report is et al., 2015). There appears to be a trade-off between the
widespread. However, we do know that lichens show large flexible and rapid moisture-uptake strategy characteristic of
within-species variability. For example, thallus nutrient thin chlorolichens that utilize humid air every night, and
concentration, a functional trait known to be important in the conservative water-storage strategy of cyanolichens that
driving thallus decomposability (Lang et al., 2009; Asplund limit their photosynthesis to rarer rainy periods (Gauslaa,
& Wardle, 2013), can show tremendous variation not Coxson & Solhaug, 2012). In lichen-dominated epiphytic
only across but also within species (Palmqvist et al., 2002; communities, there is a need for frequent rain to sustain
Asplund & Wardle, 2014). This high intraspecific variability high cyanolichen and cephalolichen biomass and thus high
is linked to the considerable ability of lichens to absorb N2 -fixation rates. Epiphytic lichens may play an important
and accumulate nutrients from atmospheric sources (Nash, role in the partitioning of moisture derived from precipitation
2008). Likewise, several studies have revealed that STM and thus the humidity of the forest interior (Van Stan &
can show considerable variation within species (Snelgar Pypker, 2015). In some sites with low rainfall, fruticose

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6 Johan Asplund and David A. Wardle

epiphytic lichens absorb moisture from fog and thereby Kaasalainen et al., 2012), although the ecological role of these
supply underlying soils with water, in turn enhancing the toxins is not well established.
availability of soil moisture for tree growth (Stanton & Horn,
2013; Stanton, Armesto & Hedin, 2014).
III. HOW VARIATION AMONG LICHENS
(5) Pigmentation AFFECTS ECOSYSTEM NUTRIENT AND CARBON
FLUX
Lichens vary hugely in colour from almost white to
black. This variation in spectral characteristics results in
large differences in thallus surface temperatures (Kershaw, (1) Biogeochemical nutrient cycling
1975; Gauslaa, 1984). As such, in cold environments While plant-dominated communities obtain most of their
dark-pigmented lichens may elevate temperatures above nutrients from the soil or from nutrients cycled within
0◦ C and induce melting of the surrounding snow, thereby the system, lichen-dominated ecosystems obtain a relatively
enabling them to utilize snow-melt water (Kershaw, 1983). large part of their nutrients from outside the ecosystem.
Variation in pigmentation among lichens may also affect This is because lichens lack roots and instead take up
microclimate at the soil surface (Kershaw, 1978). As such, the significant nutrient pools from wet and dry depositions that
light-coloured, mat-forming lichens can increase the albedo originate primarily from outside the ecosystem. They do this
of the land surface by around 1% (Stoy et al., 2012). Further, efficiently because they have a large surface area relative
it has been shown that converting closed-canopy coniferous to their biomass, and because their surfaces lack cuticles
forests to open lichen woodlands in eastern Canada would and stomata, which make them very effective at absorbing
result in a net radiative forcing of about −0.12 nW m−2 ha−1 , nutrients. In addition, lichens can accumulate concentrations
which may be of sufficient magnitude to contribute to of these captured nutrients that are vastly in excess of their
atmospheric cooling (Bernier et al., 2011). Further, the surface physiological needs. However, lichens differ tremendously in
and internal temperature of limestones are higher below the their capacity to capture nutrients from outside the ecosystem
black-coloured Verrucaria nigrescens than below the light-grey and this depends on their characteristics. Some lichen growth
V. baldensis, and the darker colour contributes to increased forms, especially fruticose hair-like lichens, are particularly
rock weathering (Carter & Viles, 2003, 2004). effective at capturing both dew and fog, which often contain
more nutrients than rain (Nash, 2008). For example, the
epiphytic chlorolichen Ramalina menziesii in an oak woodland
(6) Carbon-based secondary compounds
was shown to capture 2.85 and 0.15 kg ha−1 year−1 of N
There is considerable variation among lichens in their and phosphorus (P), respectively, from sources outside the
production of carbon-based secondary compounds (CBSCs), ecosystem (Knops, Nash & Schlesinger, 1996). Another study
and more than 800 compounds have been described (Huneck showed that this species alone was responsible for 13% of the
& Yoshimura, 1996; Huneck, 2001). These are commonly total annual canopy turnover of N, 4% of P, 7% of potassium
weak phenolic acid derivatives and all are produced by the (K), 1% of calcium (Ca), 3% of magnesium (Mg) and 8%
fungal partner. Most of them are unique to lichenized fungi of sodium (Na) (Boucher & Nash, 1990). Further, fruticose
with only a few also produced by non-lichenized fungi. These lichens, which have a relatively large surface area, appear
compounds have likely evolved to protect the lichens from a to be better at capturing elements than are foliose lichens
suite of physical and biotic stressors, such as light damage and (Yemets, Solhaug & Gauslaa, 2014). However, foliose lichens
attack by predators and pathogens (Lawrey, 2009; Solhaug are generally richer in N, P and Ca than are fruticose lichens
& Gauslaa, 2012). Further, they likely play a key role in (Mangelson et al., 2002; Asplund & Wardle, 2013). Because
driving lichen-mediated ecosystem processes and community of their capacity to take up and accumulate nutrients, lichens
assembly (Asplund, Bokhorst & Wardle, 2013; Asplund & can in some ecosystems store a substantial proportion of
Wardle, 2013; Asplund et al., 2015a). These CBSCs are often the total nutrients present in the ecosystem. For example,
present in concentrations ranging from 1 to 5% of thallus in an open Picea mariana woodland in northern Québec,
dry mass, but in the widespread epiphyte Hypogymnia physodes mat-forming terricolous lichens covering 97% of the ground
can reach over 20% (Solhaug et al., 2009). Considerable surface contained up to 20% of the total biomass, 25% of
variation in CBSC concentration exists not only across but the N and 12% of the P in the ecosystem (Rencz & Auclair,
also within lichen species (Culberson & Culberson, 1958; 1978; Auclair & Rencz, 1982).
McEvoy, Gauslaa & Solhaug, 2007; Vatne, Asplund & Approximately 10% of all lichen species contain N2 -fixing
Gauslaa, 2011; Asplund & Wardle, 2014). For instance, cyanobacteria. Because lichens often grow in nutrient-poor
concentrations of CBSCs in the lichen Lobaria pulmonaria ecosystems, those containing cyanobacteria can greatly
varies from 0.7 to 13% depending on thallus size, elevation increase the inputs of N to the ecosystem. For instance,
and pH (Asplund & Gauslaa, 2007; Vatne et al., 2011). In Pseudotsuga menzeisii forests in Oregon support a high
addition to phenolic compounds, some cyanobacteria (Nostoc abundance of the N-fixing Lobaria oregana that contributes
sp.) in lichen symbioses produce microcystins which are a approximately 50% of the total ecosystem N input (Denison,
group of cyclic peptide hepatotoxins (Oksanen et al., 2004; 1973). Further in a synthesis of 17 studies, Nash (2008)

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How lichens impact on communities and ecosystems 7

lists estimations of lichen N2 fixation contributions to the N proteins, chitin and nucleic acids (Dahlman et al., 2003)
economy for various ecosystems. These values vary from which can be solubilized and rapidly leached during the
0.04 to 0.21 kg N ha−1 year−1 in tundras and forests in early stages of the decay process (Rai, 1988). By contrast,
subarctic Alaska in which Peltigera spp. is the dominant lichen rapid release of N during decomposition was not found
(Gunther, 1989) to 16.5 kg N ha−1 year−1 in old-growth to occur for two chlorolichens, i.e. Alectoria sarmentosa and
Pseudotsuga forests in northwest USA in which Lobaria oregana Platismatia glauca, probably because of their low initial N
is dominant (Antoine, 2004). However, Nash (2008) also concentration (Campbell et al., 2010). Meanwhile, Asplund
notes that most estimates (particularly the highest ones) are & Wardle (2013) did not find any difference in N release
somewhat inaccurate and may be unreliable due to various during decomposition between N2 -fixing and non-N2 -fixing
methodological flaws. lichens. Lichen growth form also seems to play a role
in the release of N. For example, Asplund et al. (2013)
(2) Litter decomposition found that epiphytic fruticose lichens, which have a large
surface area, release more N than do epiphytic foliose
There is a substantial literature focused on understanding lichens during decomposition, despite the higher initial N
how vascular plant traits and litter quality govern variation
concentration of foliose lichens. They also found that most
in litter decomposition rates among plant species, and
foliose lichens growing on rocks rapidly lost N but this was
these show decomposition to be associated positively
probably due to many of them having a high initial N
with nutrient concentrations and specific leaf area, and
concentration. Further, P has been shown to be released
negatively with concentrations of lignin and secondary
quickly during decomposition from a variety of species of
defence compounds and leaf dry mass content (Cornelissen
lichens, including cyano-, cephalo- and chlorolichens (Caldiz
et al., 1999; Pérez-Harguindeguy et al., 2000; Cornwell et al.,
et al., 2007; Campbell et al., 2010; Asplund et al., 2013), and
2008; Makkonen et al., 2012). However, although several
most of the P in the thallus is frequently released within
studies have quantified rates of decomposition of lichen litter
5 months (Campbell et al., 2010; Asplund et al., 2013). By
in sub-tropical, temperate and boreal ecosystems (Wetmore,
1982; Guzman, Quilhot & Galloway, 1990; Knops et al., contrast, litter of Cladonia spp. growing on nutrient-poor
1996; Esseen & Renhorn, 1998; Coxson & Curteanu, 2002; soils can retain or even accumulate P during decomposition
Caldiz, Brunet & Nihlgård, 2007; Campbell, Fredeen & (Moore, 1984; Asplund et al., 2013). Other elements such
Prescott, 2010), these have each considered too few species as K which are present as dissolved monovalent ions can
to enable reliable evaluation of which lichen functional also be readily released early during the decomposition of
traits are important in regulating decomposition. However, lichen thalli (Caldiz et al., 2007; Campbell et al., 2010) in
two recent comparative studies have shown that lichen much the same manner as is often observed during plant
decomposition is related to a spectrum of thallus traits litter decomposition (Lousier & Parkinson, 1978).
that are broadly analogous to leaf traits known to regulate A vast body of literature has explored the impact of
vascular plant litter decomposition. Specifically, Lang et al. soil invertebrates on vascular plant litter decomposition
(2009) found lichen litter decomposition to be positively (Petersen & Luxton, 1982; Kampichler & Bruckner,
related to levels of thallus metabolic carbohydrates, lipids, N, 2009), and has revealed that these effects are driven by
Ca, K, pH and amino acids, while Asplund & Wardle (2013) invertebrates consuming and fragmenting litter, dispersing
showed lichen decomposition to be related to thallus N, P microbial propagules, and stimulating soil microbial activity
and pH. Further, Asplund & Wardle (2013) showed through (Parkinson, Visser & Whittaker, 1979; Seastedt, 1984). By
removing thallus CBSCs by means of acetone rinsing that contrast, only a few studies have investigated whether
CBSCs are powerful regulators of lichen decomposition, and lichenivorous invertebrates may play a role in lichen
that all CBSCs that reduced decomposition also deterred decomposition. For instance, McCune & Daly (1994) found
lichenivorous snails. They also found foliose lichens to half-lives of decomposing lichen litter to be 2–9 times
decompose quicker than fruticose ones, which probably is shorter in the presence of animals larger than 1 mm than
due to their higher N content. Finally, few studies on lichen when these were excluded. Similarly, Hypogymnia physodes
decomposition have been performed in many regions in thallus litter decomposed 1.9 times faster when animals
which they are highly abundant; for example no study has sized 0.5–3 mm had access to it (Biazrov, 1995). Further,
been conducted in dryland ecosystems despite their global Asplund et al. (2013) showed that micro-arthropods can
extent and the potentially major role of lichens in driving increase decomposition rates of lichens, but that their effects
their C cycle (Maestre et al., 2013). can be mitigated by high levels of CBSCs in the lichen
The rate at which N is released from lichens during thalli that deter lichen-feeding activity. Some lichen CBSCs
decomposition also varies between lichens with differing degrade fairly quickly during thallus senescence, suggesting
functional characteristics. For instance, Campbell et al. that they only impact micro-arthropods during the early
(2010) found N to be released quickly without initial N stages of decomposition (Asplund & Wardle, 2012). However,
immobilization from the N-fixing lichens Lobaria pulmonaria other compounds are more recalcitrant and thus increase in
and Nephroma helveticum. They argued that the relatively high concentration relative to thallus litter mass, and are therefore
N mineralization rates from these lichens may be due to likely to have longer term effects on micro-arthropod feeding
the lack of lignin and the fact that their N occurs in labile activity (Bidussi, Solhaug & Gauslaa, 2016).

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8 Johan Asplund and David A. Wardle

Some studies that have quantified decomposition rates of during decomposition when in the presence of lichen litter,
lichen and vascular plant litter in the same study have despite the lichen litter decomposing more quickly than the
shown that lichen litter often decomposes more slowly oak litter (Knops et al., 1996). This was proposed to be due
(Moore, 1983, 1984; Wardle et al., 2003). However, the to the dominant lichen R. menziesii having a poor water
lichen species that have been used in these comparisons retention capacity, leading to the decomposer community
(i.e. Cladonia spp.), have thalli that are very nutrient poor being more impeded by moisture limitation (Matthes-Sears,
and generally decompose considerably more slowly than do Nash & Larson, 1986a,b). By contrast, Vaccinium myrtillus
thalli from most other lichen species (Asplund & Wardle, litter decomposed more quickly in Cladonia mats than when
2013). In a litter-bed experiment comparing decomposition the lichens had been removed, likely because of a more
rates of 27 bryophytes, 17 lichens and 5 vascular plants, favourable microclimate and moisture conditions in the mats
lichens overall had comparable decomposition rates to those (Stark et al., 2000). Meanwhile Wardle et al. (2003) found that
of vascular plants, whereas bryophytes had the slowest vascular plant litter decomposition was largely unaffected
decomposition (Lang et al., 2009). Meanwhile, Vogt et al. by whether or not it was mixed with litter from the lichen
(1983) found that the pendulous epiphytic lichen Alectoria Cladonia stellaris, although the decomposition of the lichen
sarmentosa decomposed much more quickly than associated litter was impeded by the vascular plant litter. However, too
vascular plant litter. few studies have been performed to determine what types
Like plant leaves, epiphytic lichen material falls to the of lichens, or what lichen characteristics, exert the greatest
ground before decomposing. A number of studies have positive or negative effects on other litters, or the role of
quantified litter-fall of lichens, primarily in temperate and environmental context on these effects.
boreal forests (e.g. Esseen, 1985; Knops et al., 1996; Stevenson
& Coxson, 2003; Caldiz & Brunet, 2006). However, because
lichen litter usually falls in clumps and is therefore spatially
scattered, lichen litter-fall is often underestimated (McShane, IV. HOW VARIATION AMONG LICHENS
AFFECTS THEIR INTERACTIONS WITH
Carlile & Hinds, 1983). In temperate and boreal regions
CONSUMERS
the majority of lichen litter-fall occurs during autumn and
winter and especially during stormy events (Esseen, 1985).
This litter-fall varies hugely between stands, and lichen litter (1) Lichen food webs
deposition of between 13 and 320 kg ha−1 year−1 has been Despite the antibacterial and antifungal properties often
reported (Caldiz & Brunet, 2006; Campbell et al., 2010; ascribed to their CBSCs, lichens provide microhabitats
Rawat, Upreti & Singh, 2011). This variation mainly reflects for numerous eukaryotic and prokaryotic microorganisms
the standing crop in the stand and especially that of pendulous (Lawrey & Diederich, 2003; Grube & Berg, 2009) which
lichens which tend to fragment more easily than do other may vary greatly among lichen species (Bates et al.,
fruticose and foliose lichens. As such, the annual turnover of 2011). Indeed, recent work has highlighted the role of
pendulous lichens is commonly 10% (and up to 30%) of the lichen-associated bacteria as an important component of
standing crop, while the turnover of foliose lichens is usually the lichen meta-organism, challenging the traditional view of
a few per cent (Stevenson & Coxson, 2003). However, we are lichens simply being a symbiosis between a fungus and one
not aware of any studies explicitly comparing lichen growth or two photobionts (Aschenbrenner et al., 2016). Bacterial
rate among multiple lichen species, and it is therefore difficult cell densities in lichens dramatically exceed those in or on
to generalize about how lichen growth rates vary in relation vascular plant leaves (Cardinale et al., 2008; Grube et al.,
to functional characteristics or groupings. 2009; Saleem, 2015), and they likely play an important role
Because epiphytic lichen litter is generally more in lichen-mediated food webs through serving as food for
nutrient-rich than tree leaf litter, its role in nutrient cycling nematodes and protozoa. Bacteria varies hugely in numbers
is disproportionate to the biomass of its litter-fall. For and diversity between lichen species, and this is largely driven
example, in an oak woodland, litter inputs from the dominant by differences in lichen growth form and photobiont type
non-N-fixing lichen Ramalina menziesii was found to contain (Hodkinson et al., 2012). The variation with photobiont type is
twice as much N as oak leaf litter (Knops et al., 1996). likely to be due to the green algal symbionts providing mainly
The relatively high nutrient concentrations in lichen litter sugar alcohols and the cyanobacterial symbionts providing
compared with vascular plant leaf litter are in part because glucose, and because only the cyanobacteria provide N
plants remobilize and resorb their nutrients before leaf through biological fixation (Elix & Stocker-Wörgötter, 2008).
abscission, which lichens cannot. However, mat-forming There is evidence that species-specific differences in the
lichens continuously die off at the bottom creating necromass bacterial communities between lichen species is due in large
which leads to nutrients in the senescing parts then being part to thallus hydrophily (Wedin et al., 2016). Effects of
partially recycled internally, leading to less nutrients being hydrophily on bacteria are also observed within lichens; for
released to the ecosystem (Crittenden, 1991). example, the interior hydrophilic surfaces of Cladonia arbuscula
The presence of lichens, either when alive or as litter, can support more bacteria than its external hydrophobic surfaces
also affect the decomposition of associated plant litter. For (Cardinale et al., 2008). Bacterial symbionts can contribute
instance, oak leaf litter was found to lose mass less rapidly functionally to the lichen by providing resistance to biotic

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How lichens impact on communities and ecosystems 9

Reindeer/caribou

Mega-scale (>50.0 mm) Rodents

Monkeys

Snails

Increasing role of direct consumption

Increasing role of habitat provision

Slugs
Macro-scale (2.0–50.0 mm)
Beetles

Moth larvae

Mites
Meso-scale (0.1–2.0 mm)
Springtails

Tardigrades

Bacteria
Micro-scale (<0.1 mm)
Protozoa

Nematodes

Fig. 3. A wide range of consumer organisms depend on lichens, and these range in size from microorganisms to large mammals.
As such, lichen–consumer interactions operate at a wide range of spatial scales. For smaller organisms the primary role of lichens is
in providing a habitat, while for larger organisms their primary role is as a food source.

and abiotic stresses, biosynthesis of vitamins, detoxification substrates, and lichens that grow on rocks supported a
of inorganic substances (e.g. arsenic, copper and zinc) and much higher density of omnivorous nematodes than did
nutrient supply including N2 -fixation (as reviewed by Grube, epiphytic and terricolous lichens. Bokhorst et al. (2015) also
Cardinale & Berg, 2012; Aschenbrenner et al., 2016). found large differences in nematode community composition
The lichen thallus hosts aquatic microfauna (i.e. those that between lichens with and without N2 -fixation capability, due
live in water films), such as nematodes, protozoa, rotifers in part to higher abundances of bacterial-feeding nematodes
and tardigrades (Fig. 3) (Gerson & Seaward, 1977). As such, in N2 -fixing lichens that are adapted for feeding on their
there are complex food webs inhabiting the lichen thallus. For cyanobacterial symbionts.
instance, fungal-feeding nematodes likely feed on the lichen Further, a diverse group of terrestrial invertebrates feed on
mycobiont while bacterial-feeding nematodes (which can be and seek shelter on or in lichens (Fig. 3). These include species
abundant in lichen thalli; Bokhorst et al., 2015) feed on various of gastropods, springtails, mites, beetles, moth larvae and
bacterial symbionts. There is also a relatively high abundance woodlice (Gerson & Seaward, 1977). Further, lichenivorous
of predacious nematodes at least in epiphytic foliose lichens psocids and mites are fed upon by both pseudoscorpions
(Bokhorst et al., 2015), and these are likely to feed on various and true bugs that live on the lichens (Gerson & Seaward,
lichen-associated microfauna. The knowledge of how these 1977). Among lichenivorous invertebrates, gastropods play
aquatic faunal communities varies between lichens is limited, a particularly important role, and Asplund (2010) lists 64
although densities of rotifers and tardigrades are greater on species of terrestrial gastropods known to feed on lichens.
lichen species that have a higher biomass (Stubbs, 1989). Lichenivorous gastropods are found worldwide and feed on
Further, Bokhorst et al. (2015) showed that the diversity, but calcicolous lichens in limestone grasslands (e.g. Fröberg, Baur
not the abundance, of lichen-associated nematodes increases & Baur, 1993) or rocky deserts (Shachak, Jones & Granot,
with increasing thallus mineral nutrient concentration. They 1987), on foliicolous lichens in tropical rainforests (Lücking
also showed large differences in nematode community & Bernecker-Lücking, 2000) and on epiphytic lichens in
composition between lichens that occupy different growth temperate broadleaved and boreal forests (Asplund et al.,

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10 Johan Asplund and David A. Wardle

2010b). A few snail species are specialized lichen-feeders springtails relative to mites than did fruticose lichens. These
or feed predominantly on lichens (Kerney, 1999), and thus studies in combination point to lichen growth form as an
depend heavily on lichens as a food resource. Some snails important regulator of both the abundance and community
even have specialized radulae that enable them to graze composition of microarthropods (André, 1985). A possible
off epi- and endolithic lichens from rocks (Schmid, 1929; explanation for the higher abundance of invertebrates on
Breure & Gittenberger, 1981). Further, the foliose lichen foliose compared with fruticose lichens is the favourable
Xanthoria parietina provides the snail Balea perversa with all microclimatic conditions and shelter provided by the inter-
essential elements and nutrients necessary for its growth and face between the lichen thallus and its substrate (Søchting
reproduction (Baur & Baur, 1997). In addition to serving & Gjelstrup, 1985). In this light, springtails may completely
as a food source, lichens provide gastropods with shelter cover the underside of those foliose lichens that provide them
from predators and desiccation. For instance, B. perversa seeks with both food and shelter (Leinaas & Fjellberg, 1985).
protection under thalli of X. parietina that also serves as its food The importance of lichens in driving invertebrate
supply (Baur & Baur, 1997). Some snails may also use lichens communities is further demonstrated by the positive
to conceal themselves; for example the desert snail Napaeus correlation often observed between arthropod density and
barquini actively covers its shell with lichens (Allgaier, 2007). biomass of lichens across communities (Stubbs, 1989;
Snails show clear preferences for different lichen species Pettersson et al., 1995; Gunnarsson, Hake & Hultengren,
based on the functional characteristics of the lichens (Baur, 2004). This is true both for arthropods that feed on
Baur & Fröberg, 1994; Asplund et al., 2010b; Asplund & lichens such as mites and springtails, and for higher
Wardle, 2013). Co-existing snail species may prefer different trophic levels, such as spiders. The greater spider density
lichen species, and weight increase in juvenile snails varies in communities that support a higher biomass of epiphytic
greatly depending on which lichen species the snails are lichens has been explained in terms of lichens increasing
fed (Baur, Baur & Fröberg, 1992; Fröberg et al., 1993; the structural complexity of the habitat (Gunnarsson et al.,
Baur et al., 1994). A major driver of lichen palatability is 2004). However, lichens with identical structural complexity
their secondary chemistry; the presence of CBSCs is an can support different densities of spiders through supporting
important determinant of lichen palatability and the removal contrasting amounts of prey (i.e. lichenivorous springtails),
of CBSCs greatly increases the consumption of lichens due to variation in defence compounds (Asplund et al., 2015a).
by snails (Gauslaa, 2005; Pöykkö, Hyvärinen & Bačkor, Likewise, passerine birds that feed on invertebrates are more
2005; Černajová & Svoboda, 2014), as we discuss below. abundant in forests that support a high lichen biomass due
Furthermore, Asplund & Wardle (2013) found that generalist to increased abundance of prey (Pettersson et al., 1995).
snails preferred fruticose to foliose lichens, and foliose Lichens are also utilized by vertebrate fauna (Fig. 3).
chlorolichens over cephalo- and cyanolichens. Meanwhile, A number of bird species use lichens as nesting material or as
unlike what is often found for vascular plants (Mattson, camouflage or decoration (Richardson & Young, 1977). In
1980), Asplund & Wardle (2013) did not find any relationship addition, flying squirrels make nests of lichens, predominately
between thallus consumption by snails and concentrations of fruticose lichens of the genus Bryoria, on which they also feed.
thallus N or P across 28 forest lichen species. Further, Asplund A number of mammals feed to varying extents on lichens in
et al. (2010a) found that lichens exposed to N fertilization different regions of the world, including deer (Cervidae), elk
(and which were more N-rich) were actually less preferred (Cervus elaphus), ibex (Capra spp.), gazelle (Gazella spp.), musk
by lichenivorous gastropods. They attributed this to lower ox (Ovibos moschatus), mountain goat (Oreamnos americanus),
supply of energy in terms of mannitol in fertilized thalli. By polar bear (Ursus maritimus), lemming (Lemmus spp.), vole
contrast, Asplund, Gauslaa & Merinero (2016) showed that (Myodes spp.), marmot (Marmota spp.), squirrel (Sciuridae) and
snails prefer thalli from L. pulmonaria that had a lower C:N monkeys (Seaward, 2008). Of these, reindeer and caribou
ratio as a consequence of infection by the parasitic fungus (Rangifer tarandus; hereafter reindeer) that inhabit circumpolar
Plectocarpon lichenum. northern latitudes are especially dependent on lichens. As
Lichen traits also affect communities of other such the winter diet of reindeer is more than 50% lichen
lichen-associated invertebrates. For instance, Bokhorst et al. material, and these include mat-forming as well as epiphytic
(2015) found that thallus nutrient status (i.e. N concentration and saxicolous lichens (Scotter, 1967; Gaare & Skogland,
and N to P ratio) positively affected the diversity and abun- 1975; Boertje, 1984). The vast majority of lichens consumed
dance of both mites and springtails and also altered their by reindeer are fruticose, and mainly of the genera Cladonia,
community composition. Consequently, N2 -fixing lichens, Bryoria, Alectoria and Stereocaulon (Holleman & Luick, 1977;
which are richer in nutrients, tended to support more (and Danell et al., 1994). These species are common in reindeer
different species of) springtails and mites. Several studies have habitats and their growth form makes them easily accessible.
also shown that foliose lichens usually support more spring- Similar to reindeer, snub-nosed monkeys (Rhinopithecus bieti)
tails and mites than do fruticose or crustose lichens (André, inhabiting north-western Yunnan, China depend on lichens
1983, 1984, 1986; Colloff, 1988; Bokhorst et al., 2015), as winter fall-back food; during seasons with low food
although André (1984) found high numbers of the mite Dome- availability, lichens can constitute up to 97% of their diet
torina plantivaga in crustose lichens only. Further, Søchting & (Grueter et al., 2009). These monkeys prefer fruticose lichens
Gjelstrup (1985) found that foliose lichens supported more such as U. longissima and Bryoria spp. which are easy to grab,

Biological Reviews (2016) 000–000 © 2016 Cambridge Philosophical Society

How lichens impact on communities and ecosystems 11

and only occasionally feed on the smaller foliose lichens cephalodia rather than the green-algal parts of the thallus,
(Kirkpatrick, 1996; Grueter et al., 2009). Because of their but when CBSCs are removed by acetone rinsing, slugs do
preference for Usnea longissima, these monkeys tend to occupy not discriminate between the two parts (Asplund & Gauslaa,
relatively high and cold elevations where lichens are more 2010). The high grazing susceptibility of cephalodia in this
abundant than in the milder lowland (Grueter et al., 2012). species may explain why it is restricted to northern and
high-elevation locations that support few gastropods. Several
(2) Defence lichen species have higher concentrations or even other
types of CBSCs in their reproductive structures such as
In the 19th century, Zukal (1895) suggested that CBSCs soralia and ascocarps (Imshaug & Brodo, 1966; Brodo &
in lichens serve as defences against lichenivores. However, Hawksworth, 1977; Tønsberg, 1992; Hyvärinen et al., 2000;
Zopf (1896) found that snails did not discriminate between Asplund et al., 2010c). As such, snails completely avoid the
potato slices smeared with lichen CBSCs and those without soralia of Lobarina scrobiculata which contains five times as
CBSCs. A few years later Stahl (1904) found that removal of much m-scrobiculin than the rest of the thallus (Asplund
CBSCs by a sodium bicarbonate solution made the lichen
et al., 2010c). Meanwhile, in the absence of CBSCs, snails
more attractive to the snail Cepaea hortensis. More recent
are instead more likely to attack the soralia than the somatic
studies have utilized 100% acetone to non-destructively
parts of the thallus. This is in line with the optimal defence
remove CBSCs from living air-dry lichens; this enables
theory which predicts that the parts of an organism that are
comparisons between lichen material which does versus does
more likely to be attacked and are more important for species
not have CBSCs present (Solhaug & Gauslaa, 1996, 2001).
fitness (e.g. reproductive parts) are typically better defended
This approach provides a unique way to test the role CBSCs
against consumers (McKey, 1974; Rhoades, 1979).
play in lichen–invertebrate interactions while avoiding other
Many lichen species are represented by different
confounding factors, and it has been used in several studies
chemotypes, i.e. morphologically identical conspecifics
to show that lichen CBSCs do indeed deter invertebrates
(Reutimann & Scheidegger, 1987; Gauslaa, 2005; Pöykkö containing different groups of CBSCs, and these chemotypes
can be used for studying the ecological role of CBSCs.
et al., 2005; Asplund & Wardle, 2013; Černajová & Svoboda,
2014; Asplund et al., 2015a). For instance, Gauslaa (2005) As such, thalli of one Lobaria pulmonaria chemotype contain
offered the snail C. hortensis a choice between lichens with and high amounts of total CBSCs including stictic acid and
without CBSCs and found a significant preference for the small amounts of constictic, norstictic, peristictic and methyl
acetone-rinsed thalli in 14 out of the 17 tested lichen species. norstictic acid, while another contains low total CBSCs and
Meanwhile, Pöykkö et al. (2005) found higher survival rates only norstictic acid (Asplund, 2011a). When growing on the
of larvae of the moth Eilema depressum when reared on same trees, the chemotype with the higher total CBSCs
acetone-rinsed Vulpicida pinastri and Hypogymnia physodes than was not grazed by gastropods while the chemotype with
on control (non-rinsed) thalli, but found no effect of acetone only norstictic acid was heavily grazed. This pattern was
rinsing on survival rates on Parmelia sulcata and Xanthoria pari- later confirmed in a laboratory food-choice experiment, and
etina. The effect of acetone rinsing is highly variable between reveals that natural variation in CBSCs at the within-species
lichen species because CBSCs vary hugely both qualitatively level can serve as an important determinant of their
and quantitatively among them. In general, CBSCs that are susceptibility to grazing by gastropods (Asplund, 2011a).
restricted to the cortical layer, such as atranorin, parietin and Despite the clear effect of experimentally reducing
usnic acid and that protect the lichen from high solar radi- concentrations of CBSCs on lichen palatability, variation
ation, are less effective against lichenivorous snails (Gauslaa, in palatability among lichen species does not appear to
2005, 2009; Asplund, Solhaug & Gauslaa, 2010c). By be closely related to the total concentration of CBSCs
contrast, some medullary CBSCs are very effective against (Asplund & Wardle, 2013; Bokhorst et al., 2015). This lack
lichenivores, such as the yellow vulpinic acid (Gauslaa, 2005). of relationship is likely because of qualitative differences
Lichen CBSCs not only deter lichenivores, but also control in CBSCs among species and because different compounds
how they graze lichens, which affects lichen fitness. For have different levels of biological effectiveness and contrasting
instance, various lichen feeders, e.g. springtails, moth larvae, roles. As such, a species with high concentrations of
slugs and snails, preferentially attack the cortical layer and an ineffective defence compound is likely to be more
often also the photobionts of the lichen, but stop feeding palatable than a species with lower concentrations of a
when they reach the medulla (Hale, 1972; Baur et al., 2000; very effective defence (Gauslaa, 2008). In this light, an
Bačkor, Dvorský & Fahselt, 2003; Asplund, 2011b) where accidental experiment in which the coleopteran Lasioderma
the CBSCs are often mostly concentrated (Asplund, 2011b). serricorne attacked 1440 lichen herbarium specimens showed
However, lichens that are treated with acetone, and are that the level of consumption was strongly linked to the
therefore low in CBSCs, are instead grazed perpendicular qualitative composition of CBSCs in the lichens (Nimis &
to the lichen surface which leaves distinct holes through Skert, 2006).
all the thallus layers. Further, the foliose lichen Nephroma The CBSCs in lichens can also impact consumption by
arcticum has large cephalodia (containing colonies of N-fixing mammals, but the literature on this is very limited. For
Nostoc spp.) which, unlike the surrounding medulla, lacks instance, it is known that the bank vole, Myodes glareolus,
CBSCs (Renner, 1982). As such, slugs normally attack the prefers lichens with reduced concentrations of CBSCs

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12 Johan Asplund and David A. Wardle

N2-fixation (+)
–
–

Light blocking Rock weathering (+)

(–)

Physical separation
of plant from soil (–)

O O
NH4
K+
O

Accumulation of Ca
H2O O

OH
organic layer (+)
Increased mobilization
Enhanced soil Production of of plant nutrients (+)
moisture (+) allelochemicals (–)

Fig. 4. Contrasting mechanisms by which lichens can affect the establishment and growth of plants, notably during early stages of
primary succession. Red (−) and blue (+) = negative and positive effects of lichens on plants, respectively. Illustration by Lennart
Asplund.

(Nybakken et al., 2010). Further, usnic acid, a common scope of this review. Meanwhile, how lichens regulate plant
lichen CBSC, has been reported to kill elk (Cook et al., communities has been given much less attention (Fig. 4).
2007). Reindeer, by contrast, consume large amounts of At the beginning of terrestrial primary succession, N
usnic acid-containing lichens, because they have an usnic is often the main limiting nutrient, and pioneer N2 -fixing
acid-degrading bacterium (Eubacterium rangiferina) in their plants and lichens may play an important and well-known
rumen that detoxify the lichens (Sundset et al., 2008, 2010). role in driving initial N build-up in the ecosystem. For
As such, the presence of usnic acid actually increases the example the N2 -fixing fruticose lichen Stereocaulon spp.
digestibility of lichens by reindeer (Palo, 1993). can dominate ground cover early in succession in both
subtropical lava flows (Eggler, 1971; Mueller-Dornbois,
1987) and glacial forelands (Vetaas, 1994). The N2 fixed by
lichens, and other N2 -fixing organisms, leads to N build-up
V. HOW VARIATION AMONG LICHENS that then facilitates colonization by non-N2 -fixing vascular
AFFECTS THEIR IMPACTS ON SOILS AND plants. In this light, the vascular plants, Festuca octoflora and
PLANTS Mentzelia multiflora, when grown in desert soil together with
the cyanolichen Collema sp., have been shown to grow more
The numerous ways that communities of plants (mainly quickly and contain higher tissue element concentrations of
trees) impact on lichen community assemblies, for instance N, P, K, Ca, Mg and Fe than those grown in soil without
by competition or by providing substrates and modifying the lichen (Belnap & Harper, 1995). This is both because
environmental conditions, have been very well studied the lichens concentrate essential elements in available
(Favero-Longo & Piervittori, 2010), and are outside the forms at the soil surface and because the gelatinous sheaths

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How lichens impact on communities and ecosystems 13

often associated with the cyanobacterial symbiont (e.g. Because of the rich secondary chemistry of lichens, their
Nostoc cells in Collema spp.) contain chelating compounds. CBSCs are often claimed to have allelopathic effects on
Further, non-N-fixing lichens can also enhance soil nutrient plants (Lawrey, 1986, 1995). However, studies finding an
availability; for example biological soil crust lichens in allelopathic effect of lichen CBSCs have often been made
drylands can alter soil chemistry by accumulating nutrients in the laboratory through bioassays that use unrealistically
in their thalli (Delgado-Baquerizo et al., 2015). high concentrations of CBSCs or that use water extracts
Early colonization by lichens may also induce rock that also contain many (and often unknown) compounds
weathering that in turn releases mineral elements in forms other than CBSCs. Furthermore, many of these studies have
that plants can utilize (Viles, 1995; Adamo & Violante, 2000; evaluated the allelopathic effect of lichen CBSCs on crop
Chen et al., 2000). Lichen growth form can potentially play a plant species like tomato, lettuce, maize or sunflower, that are
role in governing these rock-weathering processes. However, not naturally exposed to lichen CBSCs (Lascève & Gaugain,
although crustose lichens are more strongly adhered to the 1990; Romagni et al., 2000; Latkowska et al., 2006; Lechowski,
rock (through their entire lower surface) than are foliose Mej & Bialczyk, 2006). However, in reality very low amounts
lichens, their ability to weather rock and release nutrients of lichen CBSCs are leached to the soil because of their low
from it is not necessarily greater (Adamo, Marchetiello water-solubility (Stark, Kytöviita & Neumann, 2007), and at
& Violante, 1993). Instead, the freeze–thaw action can ecologically relevant conditions the common lichen CSBC
be larger on rock surfaces occupied by the bigger foliose usnic acid does not reach concentrations in the soil that are
lichens than those occupied by crustose lichens, which may able to impair pine seedling growth or mycorrhizal-mediated
compensate in part for their weaker connection with the rock nutrient uptake (Kytöviita & Stark, 2009). In this light,
(Adamo & Violante, 2000). Further, the chemical weathering we currently do not have a good understanding of the
of rock and release of nutrients from it may also be driven role of allelopathic interactions involving lichens in natural
by the amount and types of CBSCs produced by the lichens ecosystems, or convincing and consistent evidence that
which themselves vary tremendously both among and within allelopathic effects of lichens are actually important.
lichen species (Adamo & Violante, 2000).
Lichens have been reported to both enhance (Zamfir,
2000; Houle & Filion, 2003) and reduce (Deines et al., 2007) VI. CONCLUSIONS
vascular plant seedling establishment, and these effects of
lichens are dependent on the types of plant and lichen (1) We showed how lichens impact ecosystem processes,
species present and on environmental context (e.g. Escudero notably those that involve the fluxes of carbon and nutrients,
et al., 2007). As such, ground covered by Cladonia has and how this is in turn regulated by the considerable
been shown to stongly reduce emergence of seedlings of variation that exists for the functional characteristics of
plant species that depend heavily on light for germination lichens (Fig. 2). We also outlined how this variation impacts
(i.e. Arenaria serpyllifolia and Veronica spicata) relative to on the interactions of lichens with other primary producers
those that do not (i.e. Filipendula vulgaris and Festuca ovina) as well as with higher trophic levels, and the consequences
(Zamfir, 2000). Further, the physical environment created of this for community and ecosystem properties.
by ground-dwelling lichens may inhibit seeds and seedling (2) Our knowledge about how lichen functional traits
radicals from reaching the soil, thereby reducing seedling (both within and between species) vary among ecosystems
establishment (Deines et al., 2007). By contrast, mat-forming or across environmental gradients is limited, and this topic
lichens such as Cladonia spp. may conserve soil moisture requires further attention. Recent work suggest that lichens
and thus facilitate seedling establishment (Zackrisson et al., show massive within-species (relative to across-species)
1995, 1997). However, these lichens accumulate little organic variation, especially in comparison with vascular plants
matter, and N mineralization rates below these mats are low, (Asplund & Wardle, 2014). There is a need for studies
which leads to lower N availability under lichens compared on how this high intraspecific variation impacts on lichen
with under plants and bryophytes (Sedia & Ehrenfeld, community assembly processes and ecosystem functioning,
2005). This results in a sparser vascular plant development in the same manner that has recently been done for vascular
and a more open forest, which leads to a feedback that plants (e.g. Jackson, Peltzer & Wardle, 2013; Kumordzi
in turn benefits mat-forming lichens (Sedia & Ehrenfeld, et al., 2015). As a first step we need consensus on what traits
2003). Biological soil crust lichens, notably in dryland are important for characterizing variation among lichens and
ecosystems, influence plant communities by affecting water their ecological roles, and the development of comprehensive
availability, erosion processes and nutrient fluxes (Eldridge, global databases that synthesize these traits.
Zaady & Shachak, 2002; Maestre et al., 2002; Eldridge et al., (3) Lichens often occur in multispecies associations, yet
2010; Chamizo et al., 2011, 2016). Recently, Mallen-Cooper studies to date have almost entirely considered only the effects
& Eldridge (2016) developed methods for measuring of single lichen species. As such, in contrast to the vast amount
functional traits of soil crusts that they proposed impact of work on this topic for vascular plants (Cardinale et al.,
on soil processes, including various enzymes, sediment 2012), little is known about how lichen species associations,
capture ability, water absorptivity, height and rhizine and their functional and taxonomic diversity, affects the
length. key community- and ecosystem-level processes that they

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14 Johan Asplund and David A. Wardle

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(Received 3 May 2016; revised 14 September 2016; accepted 16 September 2016 )

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