Suppressing competitive dominants and community
restoration with native parasitic plants using the
hemiparasitic Rhinanthus alectorolophus and the
dominant grass Calamagrostis epigejos
Jakub Tesitel*,1
, Jan Mladek1,2
, Jan Hornık3,4
, Tamara Tesitelova1
, Vojtech Adamec1
and
Lubomır Tichy5
1
Faculty of Science, University of South Bohemia, Branisovska 1760, Ceske Budejovice 370 05, Czech Republic;
2
Department of Ecology & Environmental Sciences, Faculty of Science, Palacky University, Slechtitelu 241/27,
Olomouc 783 71, Czech Republic; 3
Nature Conservation Agency of the Czech Republic, Kaplanova 1931/1, Praha
148 00, Czech Republic; 4
NGO Centaurea – Society for Landscape Monitoring and Management, Stolany 53,
Hermanuv Mestec 538 03, Czech Republic; and 5
Department of Botany and Zoology, Masaryk University, Kotlarska
2, CZ-611 37 Brno, Czech Republic
Summary
1. Dominance of native or alien competitive plants causes competitive exclusion of subordinate
species and represents a major mechanism reducing biodiversity following land-use
changes. The successful competitive strategies may, however, be interfered with by parasitic
plants, which withdraw resources from other plants’ vasculature. Parasitism may strongly
reduce the growth of the dominants, which may facilitate regeneration of other species and
consequently trigger restoration of natural communities of high diversity.
2. Here, we aim to provide robust empirical evidence demonstrating this restoration potential
of parasitic plants. We present a case study testing suppressive effects of hemiparasitic Rhinanthus
alectorolophus on competitive grass Calamagrostis epigejos. In recent decades, C.
epigejos has invaded many high-nature-value semi-natural grasslands of Central Europe,
which is one of the prominent factors causing their biodiversity decline.
3. We conducted three manipulative field experiments testing the effect of sowing of R. alectorolophus
in different vegetation types infested by C. epigejos. Rhinanthus sowing was compared to different
mowing treatments recommended as the ‘best practice’ management at respective sites.
4. Rhinanthus alectorolophus established itself in most C. epigejos-dominated plots where sown.
Calamagrostis epigejos was virtually exterminated in 2 years in two of the experiments (dry meadow
and industrial area). In the wet-meadow experiment, the suppressive effect was variable as
a result of uneven establishment success of Rhinanthus. In this experiment increased mowing
intensity had an additional suppressive effect on C. epigejos. Rhinanthus also increased regeneration
potential of other species by a temporary reduction of vegetation density. Restoration of
target vegetation composition was, however, dependent on community context.
5. Synthesis and applications. We demonstrated that hemiparasitic Rhinanthus alectorolophus
is an accessible and efficient tool for targeted biological control of Calamagrostis epigejos,
with a great potential to restore infested grassland vegetation. The strong effect of Rhinanthus
is caused by interference with the underground storage and clonal growth strategy of Calamagrostis
epigejos, which are both traits that underlie its competitive ability. The potential of
native parasitic plants should be considered in restoration management of sites infested by
competitive dominants, either alien or native.
Key-words: clonal plant, competition, diversity decline, dominance, ecological restoration,
ecosystem engineering, land use change, parasitic plant, rhizome, semi-natural grassland
*Correspondence author. E-mail: jakub.tesitel@centrum.cz
© 2017 The Authors. Journal of Applied Ecology © 2017 British Ecological Society
Journal of Applied Ecology 2017, 54, 1487–1495 doi: 10.1111/1365-2664.12889
Introduction
Dominance of competitive plant species is associated with
low community diversity (Wisheu & Keddy 1992). An
increase of dominance is a major mechanism causing biodiversity
decline following land-use change (Leps 2014).
Many competitive dominants are alien invasive species
(Gioria & Osborne 2014) but native dominants may have
comparable effects on plant diversity (Somodi, Viragh &
Podani 2008; Leps 2014). Regulation of competitive dominants
and restoration of infested communities is a serious
issue in nature conservation. Optimal restoration measures
should suppress competitive dominants and simultaneously
support spontaneous recovery species-rich
communities such as high-nature-value (HNV) grasslands.
From this perspective, drastic mechanical (e.g. topsoil
removal) or chemical (herbicide application) measures do
not represent a desirable solution.
Parasitic plants, which take up resources directly from
their host’s vascular bundles may be used as biocontrol
agents suppressing the competitive dominants. This parasitic
mechanism interferes with the resource translocation
mechanism of vascular plants. As a result, parasitic plants
can display high growth rates while strongly reducing
growth of their hosts (Shen et al. 2005, 2010; Prider,
Watling & Facelli 2009; Tesitel et al. 2015). Many parasitic
plants preferentially attack hosts of high nutrient status
(Kelly 1992) or grow vigorously when attached to
faster-growing (Hautier et al. 2010) or clonal hosts
(Demey et al. 2015; Leps & Tesitel 2015). Parasitic plants
may thus inflict disproportional harm to host plant species
displaying fast growth, efficient nutrient use or clonality,
that is, traits connected to competitive ability and
local dominance (Herben, Novakova & Klimesova 2014).
Empirical support for such suppressive potential has
recently emerged, e.g. in the case of Pedicularis palustris
L. (Orobanchaceae). This root hemiparasite suppressed
dominant sedge Carex acuta L., which consequently facilitated
transformation of species-poor tall sedge fens into
species-rich transition mires (Decleer, Bonte & van Diggelen
2013). Similarly, stem-parasitic Cuscuta campestris
Yuncker (Convolvulaceae) has been demonstrated to suppress
invasive Mikania micrantha H.B.K. in South China
(Yu et al. 2008). Extensive research is being conducted on
stem-parasitic Cassytha pubescens R.Br (Lauraceae) as a
native biocontrol of invasive leguminous shrubs in Australia
(Prider, Watling & Facelli 2009; Shen et al. 2010;
Cirocco et al. 2015). While these studies indicate a general
ability of plant parasites to decrease vitality of some competitive
dominants (including alien invasives), their use as
a targeted measure in ecological restoration remains to be
evaluated.
Here, we examine the potential of plant parasitism,
namely root-hemiparasitic species Rhinanthus alectorolophus
(Scop.) Pollich (Orobanchaceae), as a targeted
restoration measure for biocontrol of the range-expanding
grass Calamagrostis epigejos (L.) Roth. Calamagrostis
epigejos is a perennial rhizomatous species widespread
across the whole of temperate Eurasia. It uses the guerrilla
strategy of clonal growth (Rebele & Lehmann 2002)
to spread rapidly in previously unoccupied communities
diversity of which is consequently reduced by competitive
exclusion of subordinate species (Somodi, Viragh &
Podani 2008; Rebele 2014). The competitive success of the
C. epigejos lies in its ability to store and translocate
resources below ground (Rebele & Lehmann 2001;
Kavanova & Gloser 2005; Gloser, Kosvancova & Gloser
2007) and high nutrient use efficiency (Yuan et al. 2005).
Despite the fact that it is relatively slow-growing (Holub
et al. 2012), the canopy height of C. epigejos still reaches
up to 100 cm and the grass accumulates a large amount
of standing biomass over the growth season (Rebele &
Lehmann 2001). Calamagrostis epigejos efficiently translocates
nutrients from senescing shoots to its roots at the
end of the growth season. As a result, its litter is nutrientpoor,
decomposes slowly and accumulates in a thick
layer, which reduces growth and establishment of other
species (Mudrak et al. 2013).
Unlike most other competitive meadow grasses (e.g.
Arrhenatherum elatius (L.) J. Presl et C. Presl, Lolium perenne
L., Dactylis glomerata L.), C. epigejos does not
require high soil nutrient availability to spread and attain
dominance in the community. Instead, it benefits from
low nutrient availability in HNV grasslands and their
low-intensity conservation management (Hakova, Klaudisova
& Sadlo 2004; Kleijn et al. 2009). Moreover, many
European HNV grasslands of low productivity (and high
diversity) have been abandoned (Leps 2014), which further
facilitates C. epigejos to attain dominance. Calamagrostis
epigejos is difficult to suppress by re-establishment
of low-intensity land use (e.g. single-cut mowing) since
this usually does not result in its substantial decrease in
the short term (Lehmann & Rebele 2002; Hazi et al.
2011). More intense restoration measures (e.g. intense
mowing) may be harmful for valuable species still remaining
in the community (Somodi, Viragh & Podani 2008).
In summary, the expansion of C. epigejos represents a
major threat to the biodiversity of Central European
semi-natural HNV grasslands, some of which are remarkable
due to the globally unparalleled species-richness at
the small spatial scale (Chytry et al. 2015). Conventional
land-use practices (mowing, grazing) applied in low intensities
(otherwise favourable for maintenance of speciesrich
grasslands) are inefficient in terms of suppressing C.
epigejos as the species is well adapted to non-frequent
above-ground disturbance by mobilising its below-ground
resources. The below-ground resource storage could, however,
be the ‘Achilles heel’ of the successful C. epigejos
strategy if susceptible to infection by a root parasitic
plant. A recent pilot experiment demonstrated the ability
of root-hemiparasitic R. alectorolophus to establish in C.
epigejos-dominated vegetation (Mudrak et al. 2014) and
form functional haustorial connections to its roots
(Fig. S1, Supporting Information).
© 2017 The Authors. Journal of Applied Ecology © 2017 British Ecological Society, Journal of Applied Ecology, 54, 1487–1495
1488 J. Tesitel et al.
Here, we follow up this pilot study by three manipulative
field experiments to demonstrate the potential of R.
alectorolophus to restore grasslands overgrown by C.
epigejos. Specifically, we test three hypotheses: (1) Rhinanthus
has the capacity to suppress C. epigejos rapidly when
sown into its stand and established, (2) Rhinanthus opens
gaps in the sward (community features known to be crucial
for seed or bud bank regeneration; Fibich et al.
2013), and (3) Rhinanthus can increase community diversity
and drive community composition towards semi-natural
HNV grasslands. Sowing of Rhinanthus was the main
and identical treatment in all experiments. We compare
its effects to mowing treatments corresponding to recommended
‘best practice’ management of respective vegetation
types at individual experimental sites (Hakova,
Klaudisova & Sadlo 2004).
Materials and methods
GENERAL EXPERIMENT LAYOUT AND SEED SOURCE
Three experiments were established in different habitats in 2012
to test the effect of sowing of R. alectorolophus on grassland vegetation
dominated by C. epigejos. Baseline data was collected
prior to any experimental treatments. Further monitoring was
done annually for the following 3 years (2 years in the case of
experiment 3, see below). Monitoring was conducted in late June/
early July to match the phenology of C. epigejos which peaks at
this time. At that time, Rhinanthus plants were senescent, mostly
in the fruiting phase with some leaves having already fallen off.
The recorded Rhinanthus cover/biomass values thus may be lower
than its peak standing crop. All plots were free of any hemiparasitic
species at the start of the experiments. Seed origin of R. alectorolophus
and the sowing approach was identical in all
experiments. The seeds were collected in a wild population
located close to Huslenky, Vsetınske vrchy Mts., Czech Republic
(49°180
58″N, 18°050
39″E, 600 m a.s.l.) and sown in the corresponding
experimental plots in October 2012; no additional sowing
was conducted in experiments 2 and 3. In addition,
experiment 1 also comprised two mowing treatments. Experiments
2 and 3 comprised sowing of legumes as an additional
treatment, which was motivated by local field observations indicating
a possible supportive effect on Rhinanthus establishment.
However, no significant effect of legumes on any of the monitored
parameters was detected. Therefore, the plots where these
were sown were removed from the data and the results are not
reported.
Experiment 1
Experiment 1 was established on an abandoned meadow close to
Svihov, Zelezne hory Mts., Czech Republic (49°500
08″N,
15°510
44″E, 440 m a.s.l.). The meadow consisted of a mosaic of
intermittently wet meadows (Molinion) and oligotrophic submontane
grasslands (Violion caninae; Chytry 2007–2013) that had
been unmanaged for at least a decade. Most of the site was overgrown
by C. epigejos with an admixture of other grasses
(Alopecurus pratensis L., Deschampsia cespitosa (L.) P. Beauv.)
but species typical of local species-rich meadows, such as Carex
hartmanii Cajander, Betonica officinalis L., Sanguisorba officinalis
L., Solidago virgaurea L., and Viola canina L. were still scarcely
present in the community.
The experimental layout consisted of six blocks each composed
of four 3 m 9 3 m plots. Whole blocks were mown in summer
(after the vegetation composition data sampling and biomass collection)
which is a standard management practice of this vegetation
type. Two experimental treatments were combined in a full
factorial design: (i) sowing of R. alectorolophus (500 seeds mÀ2
)
and (ii) an additional mowing in October (including litter removal
and gentle moss layer disturbance by raking, a treatment known
to potentially improve Rhinanthus establishment; Mudrak et al.
2014). This resulted in four treatment combinations within each
block: (i) summer mowing only (control; corresponds to recommended
conservation management), (ii) summer and autumn
mowing (corresponds to conventional restoration management of
C. epigejos-heavily infested sites), (iii) summer mowing + Rhinanthus,
(iv) summer and autumn mowing + Rhinanthus. Sowing (using
fresh seeds) and all treatments were repeated every year.
Vegetation composition of the central 2 m 9 2 m square of each
of the plots was monitored every year in late June/early July by a
visual estimate of cover (%). In addition, above-ground biomass
of C. epigejos was harvested from a 1 m 9 1 m permanent square
located within the central square to determine its dry-weight.
Experiment 2
Experiment 2 was established on a dry meadow in the northern
part of the White Carpathian Mts. (49°60
41″N, 18°030
00″E, 410
m a.s.l.). The meadow had been abandoned for approximately 40
years and regular summer mowing had restarted 8 years prior to
the experimental layout. The plant community was dominated by
C. epigejos and Brachypodium pinnatum (L.) P. Beauv., but many
dicotyledonous forbs (Centaurea jacea L., Knautia arvensis (L.) J.
M. Coult., Pulmonaria mollis Hornem., Trifolium medium L.) persisted
on the site. The site was fenced to prevent browsing of roe
deer.
The experimental layout included five blocks each composed of
two 2 m 9 2 m plots. Rhinanthus alectorolophus was sown
(500 seeds mÀ2
) onto one of the plots while the other was a control
without any sowing. Whole blocks were mown in summer
(after the vegetation composition data sampling and biomass collection),
which follows the ‘best practice’ conservation management
of this vegetation type. Vegetation composition of the
central 1 m 9 1 m square was monitored annually at the end of
June using the calibrated weight-estimate method (Tadmor et al.
1975). Species biomass estimate was based on its estimated proportion
in the community multiplied by the community biomass,
which was harvested from the same square and its dry weight
was determined.
Experiment 3
Experiment 3 was established on an abandoned site located on
the campus of the University of South Bohemia and the Biology
Centre of the Czech Academy of Science in Ceske Budejovice
(48°580
33″N, 14°260
47″E, 390 m a.s.l.). The site was unmanaged
for c. 20 years and was largely overgrown by C. epigejos. The site
was fenced which prevented access of larger wild mammals such
as roe deer or wild boars.
The experimental layout included four blocks each composed
of two 3 m 9 3 m plots. Rhinanthus alectorolophus was sown
© 2017 The Authors. Journal of Applied Ecology © 2017 British Ecological Society, Journal of Applied Ecology, 54, 1487–1495
Suppressing dominants by parasitic plants 1489
(500 seeds mÀ2
) onto one of the plots while the other plot was a
control without any sowing. Whole blocks were mown twice a
year – in summer (July) and autumn (October). Following the
autumn mowing, the litter was removed and gentle raking was
applied as in experiment 1. This mowing treatment corresponds
to the conventional restoration management suitable for sites.
Vegetation composition of the central 2 m 9 2 m square of each
of the plots was monitored every year in late June/early July by a
visual estimate of cover (%). Biomass of C. epigejos was not sampled
in this experiment; therefore the percent cover was used as a
dominance measure. The experimental site was destroyed in the
autumn of 2014 due to establishment of an arboretum. Therefore,
the monitoring could not extend to 2015.
DATA ANALYSIS
We analysed the following variables in each experiment: a measure
of dominance of C. epigejos (biomass dry weight or its estimate
or cover), which was used to test hypothesis 1, herb layer
cover relevant to hypothesis 2, and cover of Rhinanthus as an
indicator of Rhinanthus establishment. To test hypothesis 3, we
computed the Shannon diversity index (H) from the vegetation
composition data using natural logarithms of species abundances.
In addition, we computed dissimilarity of vegetation composition
of each sample to the corresponding potential target vegetation.
Vegetation composition of reference grassland types was obtained
from the Czech National Phytosociological Database (Chytry &
Rafajova 2003) from which we selected plots of intermittently
wet meadows and submontane oligotrophic grasslands (Molinion,
Violion caninae), semi-dry suboceanic grasslands (Bromion), and
mesic meadows (Arrhenatherion; Chytry 2007–2013) as targets for
experiments 1, 2 and 3, respectively. The dissimilarities were subsequently
computed as Bray–Curtis dissimilarity between composition
of individual vegetation samples and the most similar plot
in the corresponding reference set. The dissimilarities were based
on the square-root of cover (experiments 1, 3) or square-root of
biomass estimate values (experiment 2).
Mixed-effect linear models were used for all univariate statistical
analyses. Biomass and cover data were log-transformed prior
to analysis. A saturated model containing a year of sampling (recoded
as a year since the start of the experiment), all treatments
and all possible interactions as fixed effects and plot identity
nested within a block as random effects was first fitted for each
response variable. Minimum adequate models were subsequently
selected by sequential removal of non-significant fixed-effect
terms or their interactions. We retained non-significant terms, of
which interactions were significant. Significance tests of individual
regression coefficients of the final models are reported in the text.
All analyses were conducted in R, version 3.2.2 (R Core Team
2015) using R package nlme, version 3.1 (Pinheiro et al. 2015).
We also conducted multivariate constrained ordination analyses
(Smilauer & Leps 2014) of the community composition presented
in Appendix S1.
Results
EXPERIMENT 1
In the wet meadow overgrown by C. epigejos, R. alectorolophus
established in all sown plots in 2013 but its
cover was variable (Fig. S2.1 in Appendix S2). Rhinanthus
decreased slightly in 2014 followed by a steep decline in
2015. Flowering Rhinanthus plants were regularly damaged
by grazing roe deer which nibbled the inflorescences,
but this damage never occurred before flowering and
mostly affected a minor proportion of the plants. Deer
damage was only apparent on Rhinanthus; other plants
were left intact.
Biomass of C. epigejos was significantly reduced by both
sowing of Rhinanthus and mowing twice per season (Fig. 1;
Table 1). These negative effects (Rhinanthus 9 year interaction
t69 = À4Á33, P < 0Á001; mowing twice 9 year interaction
t69 = À2Á17, P = 0Á033) were additive (Table 1);
therefore the largest reduction of C. epigejos biomass was
observed in the plots where both treatments were applied.
Reduction of C. epigejos was variable among the blocks,
which was correlated with the abundance of Rhinanthus.
More than 90% decline of C. epigejos was generally
observed only in plots where Rhinanthus cover reached
20% at least once during the experimental period (Fig. 2).
The experimental block where Rhinanthus failed to reduce
C. epigejos was co-dominated by A. pratensis, a fast-growing
tall grass, which Rhinanthus apparently did not parasitise
and which probably prevented its better
establishment.
In addition to the significant suppression of C. epigejos,
Rhinanthus significantly reduced herb layer cover 2 years
after its sowing (Fig. 1; Rhinanthus 9 2014 vs. 2012 interaction
t66 = À4Á70, P < 0Á001) and increased Shannon
index (Fig. 1; Rhinanthus 9 year interaction t70 = 2Á88;
P = 0Á005). Both sowing of Rhinanthus and mowing twice
a year significantly decreased dissimilarity (i.e. increased
similarity) to target vegetation (Rhinanthus 9 year interaction
t69 = À2Á64, P = 0Á010; mowing twice 9 year interaction
t69 = À2Á20, P = 0Á031). Significant directional effect
of Rhinanthus on community composition was identified
also by a community ordination analysis (Appendix S1).
EXPERIMENT 2
In the dry meadow, R. alectorolophus established itself in
all sown plots in 2013 (Fig. S2.2 in Appendix S2). The
establishment success was rather even among the blocks.
Rhinanthus abundance did not substantially change in the
following year but a marked decline was observed in 2015
(Fig. S2.2 in Appendix S2).
Calamagrostis epigejos was strongly suppressed by the
sowing of Rhinanthus (Fig. 3, Table 1; Rhinanthus 9 year
interaction t28 = À4Á68, P < 0Á001). The suppression was
considerable already in the first year after sowing but even
more pronounced in the successive years, when the abundance
of C. epigejos declined close to zero in all plots with
Rhinanthus (Fig. 3).
Rhinanthus significantly decreased herb layer cover in
the year following its sowing (Fig. 3; Rhinanthus 9 2013
vs. 2012 interaction t24 = À2Á58, P = 0Á016) and in the
successive year (Rhinanthus 9 2014 vs. 2012 interaction
t24 = À2Á56, P = 0Á017). The herb layer cover increased
© 2017 The Authors. Journal of Applied Ecology © 2017 British Ecological Society, Journal of Applied Ecology, 54, 1487–1495
1490 J. Tesitel et al.
again in the last year of the experiment (Fig. 3). No significant
effects of Rhinanthus on the Shannon index, dissimilarity
to target vegetation or a directional change of
community composition (Appendix S1) were observed.
EXPERIMENT 3
At the abandoned site, R. alectorolophus established itself in
all sown plots in 2013 and retained its dominance also in the
following year (Fig. S2.3 in Appendix S2). As a result of
seed dispersal, few Rhinanthus plants were established at
some of the control plots in 2014 (Fig. S2.3 in Appendix S2).
Calamagrostis epigejos declined in plots of all treatments
throughout the experiment (Fig. 4; year main effect
t14 = À3Á89, P = 0Á002). However, the decline was significantly
steeper in plots with Rhinanthus (Fig. 4; Rhinanthus
9 year interaction t14 = À5Á12, P < 0Á001).
Calamagrostis epigejos cover approached zero in the second
year after sowing of Rhinanthus. There was no significant
effect of Rhinanthus on herb layer cover, the Shannon
index, dissimilarity to target vegetation or a directional
change of community composition (Appendix S1).
Discussion
All three experiments support hypothesis 1 by demonstrating
the potential of R. alectorolophus to substantially
and rapidly (in 1 or 2 years) suppress C. epigejos. The
Table 1. Summaries of minimal adequate models describing the effects of individual predictors on response variables in experiments 1–3
Exp. Response Model structure (fixed effects)†
1 Calamagrostis epigejos biomass Mowing twice + Rhinanthus + Year + Mowing twice 9 Year* + Rhinanthus 9 Year***
1 Herb layer cover‡
Rhinanthus + Year + Rhinanthus 9 Year***
1 Distance to target vegetation Mowing twice + Rhinanthus + Year + Mowing twice 9 Year* + Rhinanthus 9 Year*
1 Shannon index Mowing twice* + Rhinanthus + Year*** + Rhinanthus 9 Year**
2 Calamagrostis epigejos biomass estimate Rhinanthus + Year + Rhinanthus 9 Year***
2 Herb layer cover‡
Rhinanthus + Year + Rhinanthus 9 Year*
3 Calamagrostis epigejos cover Rhinanthus + Year** + Rhinanthus 9 Year***
†
Only models containing at least one significant fixed-effect predictor are listed.
‡
Year was used as a categorical predictor in these models.
*P < 0Á05, **P < 0Á01, ***P < 0Á001; non-significant regression coefficients are displayed in grey.
Fig. 1. Effects of the experimental treatments on Calamagrostis epigejos above-ground biomass, herb layer cover, dissimilarity of vegetation
composition to target vegetation and Shannon index in the experiment 1. Means, one standard error intervals, and data ranges are
displayed by points, bold lines, and whiskers, respectively.
© 2017 The Authors. Journal of Applied Ecology © 2017 British Ecological Society, Journal of Applied Ecology, 54, 1487–1495
Suppressing dominants by parasitic plants 1491
level of suppression is tightly linked with the establishment
success of Rhinanthus. Successful application
requires a minimum threshold abundance of the hemiparasite
(20% cover in the case of experiment 1). Rhinanthus
establishment in favourable environmental conditions can
be impeded by competition for light during its early development
(before or shortly after the attachment to the
host; Tesitel et al. 2011). Therefore, co-dominance of fastgrowing
dominants with early phenology may be a limiting
factor for Rhinanthus as indicated by one block of
experiment 1 co-dominated by fast-growing A. pratensis.
This limitation due to competition for light from fastgrowing
dominants can be expected to be strongest at
sites that are simultaneously moist and nutrient-rich
where the relative advantages provided by hemiparasitism
decrease as does the suppressive effect on the host (Tesitel
et al. 2015).
The rapid decline of C. epigejos following the establishment
of Rhinanthus was comparable to the effect of a
selective herbicide. The initial rapid increase of the hemiparasite
causing the rapid decline of C. epigejos followed
by the decline of Rhinanthus in successive years indicates
a relatively strong specificity of the hemiparasitic interaction.
The specificity is furthermore supported by the moderate
effect of Rhinanthus on the community composition
in experiment 1 and the lack of directional effects in
experiments 2 and 3. Such strong and specific interaction
may seem surprising given the widely shared view on Rhinanthus
species as generalists with preferences for grasses
and legumes (Cameron & Seel 2007). However, this view
has recently been challenged by Rowntree et al. (2014)
who demonstrated host species identity was more important
than functional group membership for the outcome
of the hemiparasitic interaction. From this perspective, C.
epigejos may be a host with traits that make it exceptionally
susceptible to hemiparasite infection. Its extensive
resource storage located in the roots (Kavanova & Gloser
2005) can be directly accessed by the hemiparasites.
Fig. 2. Effect of maximum cover of Rhinanthus alectorolophus on
the relative change of Calamagrostis epigejos above-ground
biomass between the start and the end of experiment 1. Each
experimental plot with Rhinanthus is represented by two concentric
circles. Grey circles and black circles indicate C. epigejos
above-ground biomass in 2012 and 2015, respectively. Size of the
circles is proportional to the dry mass in g mÀ2
as indicated by
the legend. Note the log-scale of the x-axis. Regression line with
confidence intervals is displayed (r2
= 0Á65, F1,10 = 18Á43,
P = 0Á0016).
Fig. 3. Effect of Rhinanthus alectorolophus on Calamagrostis
epigejos above-ground biomass estimate and herb layer cover in
comparison with single mowing control in experiment 2. Means,
one standard error intervals, and data ranges are displayed by
points, bold lines, and whiskers, respectively.
0
10
20
30
40
50
60
Year
Calamagrostisepigejoscover(%)
2012 2013 2014
control (mowing)
Rhinanthus alectorolophus
Fig. 4. Effect of Rhinanthus alectorolophus on Calamagrostis
epigejos cover in comparison with mowing-twice control treatment
in experiment 3. Means, one standard error intervals, and
data ranges are displayed by points, bold lines, and whiskers,
respectively.
© 2017 The Authors. Journal of Applied Ecology © 2017 British Ecological Society, Journal of Applied Ecology, 54, 1487–1495
1492 J. Tesitel et al.
Root-parasitism thus interferes with the key trait underlying
C. epigejos growth and competitive strategy, which
inflicts intense stress on the grass. Its relatively slow
growth and late phenology decrease the above-ground
competitive effects on hemiparasite seedlings (provided
the slowly decomposing litter layer is removed or not too
thick). Moreover, Rhinanthus growth and the massive
harm inflicted to C. epigejos were likely further increased
by the host clonality as suggested by recently formulated
clonal integration hypothesis (Demey et al. 2015; Leps &
Tesitel 2015). Experiments 1 and 2, however, indicate that
the hemiparasite population may collapse after depleting
the clonal host resources. This is crucial for the practical
use of the hemiparasites as biological control and restoration
agents because it diminishes the possibility of their
long-lasting dominance. However, it also means that the
suppressive effect on C. epigejos is rather short-term and
restoring its dominance must be prevented by standard
methods of conservation management (e.g. mowing once
a year). On a larger spatial scale than just a few square
metres, Rhinanthus can be expected to establish patch
dynamics within a site, which may result in a continuous
and spatially heterogeneous suppressive effect on C. epigejos
population.
The community effects of R. alectorolophus corresponding
to hypotheses 2 (sward opening) and 3 (a directional
community composition change and an increase of diversity)
were only observed in two or one of the experiments,
respectively. A temporary decrease of herb layer cover
induced by Rhinanthus was observed in experiments 1 and
2, that is, the semi-natural HNV grassland sites. Such
sward opening indicates potential for community composition
change towards the target vegetation type. However,
realisation of such potential differed between
experiments 1 and 2. In addition, experiment 1 has
demonstrated that the effect of the hemiparasites may be
synergic with increased mowing intensity. This variability
of the community effects was probably caused by differential
community contexts. The vegetation in experiment 1
was largely overgrown by C. epigejos. Most other species
had disappeared from the experimental plots but were still
scarcely present at the site, in the seed bank or in
dormant underground stages. Their re-appearance or
re-establishment after opening the canopy increased species-richness
up to 42 species 4 mÀ2
which approaches the
maximal recorded species-richness (51 species 4 mÀ2
) of
wet meadows in the region (Hornık et al. 2012). In experiment
2, C. epigejos was less dominant than at the start of
the other two experiments due to re-establishment of
management 8 years before. Therefore, plant diversity
had been preserved because the competitive exclusion of
subordinate species occurs only after increasing dominance
of C. epigejos (Somodi, Viragh & Podani 2008).
Experiment 3 might have been too short-lasting to
observe sward opening, although substantial gaps not
captured by the monitoring must have occurred in late
summer following the death of the Rhinanthus annuals.
The context dependency seems typical of Rhinanthus biodiversity
effects as indicated by previously observed positive
(Pywell et al. 2004; Westbury et al. 2006) or neutral
(Westbury & Dunnett 2007, 2008; Mudrak & Leps 2010)
effects of Rhinanthus minor on community diversity
despite almost universal reductions of standing crop
biomass and relative proportion of grasses.
Root hemiparasites are recognised as a functional
group with profound community and ecosystem effects
(Press & Phoenix 2005; Watson 2009; Demey et al. 2015).
Species of the genus Rhinanthus have been demonstrated
to decrease community productivity (Ameloot, Verheyen
& Hermy 2005), alter competitive relations in the communities
(e.g. Davies et al. 1997; Westbury & Dunnett 2007;
Mudrak & Leps 2010; Hellstr€om, Bullock & Pywell 2011;
Demey et al. 2015) and affect nutrient cycling (Fisher
et al. 2013; Demey et al. 2014). These effects may facilitate
temperate grassland diversification. Specifically,
native R. minor has been demonstrated to suppress grasses
and increase subordinate forbs, an effect extensively used
in grassland restoration in the United Kingdom (e.g.
Pywell et al. 2004; Westbury et al. 2006; Hellstr€om, Bullock
& Pywell 2011). However, this application of the
hemiparasites concerns the re-creation of semi-natural
grasslands on ex-arable land or restoration of grasslands
degraded by high land-use intensity (fertiliser application
mainly), that is, ecosystems in which biodiversity has been
negatively affected by human activity. The underlying
community effect of the hemiparasites is largely non-specific
as it reduces standing crop and the grass:forb ratio
(i.e. relation between broadly defined functional groups).
By contrast, complete eradication of the competitive dominant
and pronounced decrease of herb layer cover
inflicted by R. alectorolophus in our study, represent
extreme forms of these ecological effects of root
hemiparasites.
Several studies testing the impacts of other (hemi)parasitic
plants on particular competitive dominants revealed
similarly drastic and at least partially specific effects (Yu
et al. 2008; Prider, Watling & Facelli 2009; Shen et al.
2010; Decleer, Bonte & van Diggelen 2013; Cirocco et al.
2015). Such suppressive effects suggest that native (hemi)parasitic
plants may be considered as potential biological
controls of competitive dominants possibly including invasive
species. However, any such application must be
underlain by detailed knowledge of both host and parasite
biology and experimental field assays to ensure its efficiency
and minimise risks of possible adverse side-effects.
Given the profound effects of many parasitic plants on
ecosystems (Press & Phoenix 2005; Watson 2009) extensive
damage may be incurred by an alien parasitic plant;
therefore, only native parasitic plants may be considered.
Local propagule sources should be used preferably to conserve
local genetic resources. However, the lack of a clear
phylogeographic pattern in Rhinanthus species in Europe
(Vrancken, Brochmann & Wesselingh 2009, 2012) suggest
a lower importance of this rule in this particular case. A
© 2017 The Authors. Journal of Applied Ecology © 2017 British Ecological Society, Journal of Applied Ecology, 54, 1487–1495
Suppressing dominants by parasitic plants 1493
more pragmatic approach to seed origin may be considered;
e.g., the recently suggested genetic diversity
approach, which involves sowing a mixture of seeds originating
from multiple sources (Kettenring et al. 2014).
Conclusions and applications
We demonstrated the potential of R. alectorolophus to act
as a largely specific native biological control of competitive
dominant C. epigejos. Depending on the community
context, Rhinanthus may also facilitate restoration of biodiversity
of C. epigejos-infested grasslands. Our study is
one of the pioneering works to demonstrate native parasitic
plants as promising tools to control problematic,
mainly competitive, plant populations across the globe.
The parasites’ interference with the growth strategy of the
targeted competitive species underlies the strong suppressive
effect. Such targeted use of (hemi)parasitic plants
complements their current generic use to facilitate diversification
and increase forb abundance in HNV semi-natural
grassland restoration.
Authors’ contributions
J.T., J.M. and J.H. conceived the ideas and designed the methodology.
J.T., J.M., J.H., T.T. and V.A. collected the data. J.T. and L.T. analysed
the data. J.T. led the writing of the manuscript. All authors contributed to
the drafts and gave final approval for publication.
Acknowledgements
We thank Czech Science Foundation (project 14-26779P) for financial support,
Pavla Mladkova, Ondrej Nezval, Miroslav Dvorsky, David Opalka,
Eva Hola, Julie Jandova, Sarka Jiraska, Adela Krejcı, Jirı Sladky, Lukas
Svobodnık and Petra Ebermannova for field assistance, and Richard Kidd
for English revision.
Data accessibility
Vegetation composition and Calamagrostis epigejos biomass data are
available at Dryad Digital Repository https://doi.org/10.5061/dryad.4r390
(Tesitel et al. 2017).
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Supporting Information
Details of electronic Supporting Information are provided below.
Fig. S1. Anatomical section of haustorium of Rhinanthus alectorolophus
on the root of Calamagrostis epigejos.
Appendix S1. Community ordination analysis.
Appendix S2. Relative dominance of Rhinanthus alectorolophus.
© 2017 The Authors. Journal of Applied Ecology © 2017 British Ecological Society, Journal of Applied Ecology, 54, 1487–1495
Suppressing dominants by parasitic plants 1495