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Functional Ecology. 2022;00:1–13.
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1wileyonlinelibrary.com/journal/fec
Received: 3 August 2022
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Accepted: 7 November 2022
DOI : 10.1111/136 5-243 5.14232
RESEARCH ARTICLE
Parasitic plants indirectly regulate decomposition of soil
organic matter
Yongge Yuan1,2 | Xinru Lin3 | Gelv Chen3 | Mark van Kleunen1,2,4 | Junmin Li1,2,3
© 2022 The Author s. Functional Ecology © 2022 British Ecolo gical S ociet y.
1School of Advanced Study, Taizhou
University, Taizhou, China
2Zhejiang Provincial Key Laboratory
of Plant Evolu tionary Ecology and
Conservation, Taizhou University, Taizhou,
China
3School of Life Science, Taizhou
University, Taizhou, China
4Ecology, Department of Biology,
University of Konstanz, Constance,
Germany
Correspondence
Junmin Li
Email: lijmtzc@126.com
Funding information
National Natural Science Foundation of
China, Grant/Award Number: 32271630,
32271590 and 3150 0416; Zhejiang
Provincial Natural Science Foundation,
Grant/Award Number: LY21C0300 04;
Outstanding Youth Fund of Taizhou
University, Grant/Award Number:
2019YQ002; Ten Thousand Talent
Program of Zhejiang Provin ce, Gra nt/
Award Number: 2019R520 43
Handling Editor: Adam Frew
Abstract
1. Parasitic plants have been shown to affect soil- organic- matter (SOM) decom-
position, but the mechanism is unknown. As arbuscular mycorrhizal fungi (AMF)
can affect decomposition and compete with parasitic plants for carbon, we hy-
pothesized that parasitic plants can indirectly regulate SOM decomposition by
suppressing the effects of AMF on decomposition.
2. To test this hypothesis, we conducted two container experiments in which the
herbaceous plant Bidens pilosa was inoculated with the AMF Rhizophagus intra-
radices or not, and Cuscuta australis or not. In one experiment, we provided SOM
within hyphae- in- growth bags as 13C- /15 N- labelled maize leaves and in the other
experiment as phytate- P. We assessed growth and nutrient uptake of B. pilosa,
growth of C. australis, the SOM remaining in the hyphae- in- growth bags, and the
bacterial communities.
3. Parasitization increased the 13C and decreased the organic P remaining in the
bags, but only in the presence of the extraradical AMF hyphae. AMF decreased
the 13C and increased the organic P remaining in the absence of the parasite, but
not in the presence of the parasite.
4. Our results demonstrate that parasitic plants can regulate the decomposition of
organic materials indirectly by suppressing the effect of the extraradical AMF
hyphae on decomposition. In other words, parasitic plants can regulate SOM
decomposition indirectly via a multitrophic cascading effect. Our study helps to
unravel the mechanisms of a sophisticated hidden ecological process, and is an
important step forward in elucidating the roles of parasitic plants in soil nutrient
cycling.
KEYWORDS
arbuscular mycorrhizal fungi, cascading effect, decomposition, multi- trophic interactions,
parasitic plant, plant– soil interactions, soil microbes
1 | INTRODUC TION
Trophic cascades and top- down control, in which organisms at
higher trophic levels regulate organisms at lower trophic levels, are
important drivers of ecosystem processes. Great attention has been
directed toward predator- based food webs (Estes et al., 2011; Ripple
et al., 2014), but few studies have explored the role of top- down
cascades in regulating decomposition of organic matter and nutrient
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YUAN et a l.
cycling. Parasitic plants obtain part or all of their resources from their
hosts, thereby reducing host productivity (Bardgett et al., 2006;
Sui et al., 2019; Yuan et al., 2021). Parasitic plants are also known
to cause top- down cascading effects on the decomposition of
soil organic matter (SOM; Bardgett et al., 20 06; Di et al., 2017; Li
et al., 2008). For example, Bardgett et al. (2006) showed that the
hemiparasite Rhinanthus minor L. indirectly promotes nitrogen (N)
mineralization and thereby modifies the availability of mineral N rel-
ative to dissolved organic N. However, the mechanism underlying
the cascading effects of parasitic plants on decomposition of organic
matter remains unknown.
Increasing numbers of studies show that parasitic plants
can affect soil nutrient cycling (Ameloot et al., 2008; March &
Watson, 2010; Ndagurwa et al., 2014, 2015; Quested, 2008;
Spasojevic & Suding, 2011). For example, the concentrations of nutri-
ents, like N, phosphorus (P), potassium (K), calcium (Ca) and magne-
sium (Mg), in the soil beneath parasitized trees differed significantly
from those beneath nonparasitized trees (Muvengwi et al., 2015;
Ndagurwa et al., 2016). Possible explanations for this may be the
litter pathway or parasitism pathway. The litter pathway refers to the
direct input of nutrient- rich litter of the parasitic plant into the soil,
or the accelerated soil nutrient turnover of parasitic litter (Demey
et al., 2014; Ndagurwa et al., 2020; Spasojevic & Suding, 2011). The
parasitism pathway refers to the direct negative effect of the para-
site on the host plant and the subsequent cascading effects on soil
microbes and soil nutrient cycling (Bardgett et al., 2006; Press &
Phoenix, 2005; Yuan et al., 2021). For example, parasitism on host
plants can indirectly affect the microbial communities, including
arbuscular mycorrhizal fungi (AMF; Brunel et al., 2020), which may
affect nutrient cycling.
AMF form symbiotic associations with the roots of about 72% of
all plant species (Brundrett & Tedersoo, 2018). AMF acquire soil nu-
trients, especially N and P, with their mycelium and pass these on to
their host plants in return for carbon (Jiang et al., 2017; Luginbuehl
et al., 2017). Previous studies suggested that AMF can also af-
fect nutrient availability by promoting (Cheng et al., 2012; Hodge
et al., 2001) or inhibiting (Carrillo et al., 2016; Leifheit et al., 2015)
decomposition of SOM. However, the underlying mechanism is still
unclear. One hypothesis is that AMF do not have any saprotrophic
capability themselves, but that they influence associated micro-
bial decomposers (Cheng et al., 2012; Hodge et al., 20 01; Schäfer
et al., 2019; Verbruggen et al., 2016). For example, AMF could carry
and enrich microbial decomposers, and affect their activity by pro-
viding them with carbon (C; Jansa & Hodge, 2021; Jiang et al., 2021;
Zhang, Xu, et al., 2016) or by changing the physicochemical environ-
ment (Ding et al., 2 014; Wang et al., 2013). In line with this hypoth-
esis, Zhang, Xu, et al. (2016) found that AMF can provide C for the
growth and activity of phosphate- solubilizing bacteria. On the other
hand, Jannoura et al. (2012) repor ted that in N- deficient soil, the
presence of AMF can decrease N supply to microbial decomposers,
and thereby reduce SOM decomposition.
Several studies have shown that AMF can not only affect the
strength of the direct negative effect of parasitic plants on their host
plants (Li et al., 2013; Sui et al., 2019), but that they could also cascade
effects of parasitic plants to other trophic levels (Yuan et al., 2021).
For example, the stem holoparasite Cuscuta australis R.Br. can in-
directly affect growth of neighbouring unparasitized plants via the
belowground hyphal bridges connecting host and neighbouring
plants (Yuan et al., 2021). Because both parasitic plants and AMF
obtain C from their host plants (Bardgett et al., 2006; Brundrett &
Tedersoo, 2018), the C obtained by parasitic plants may decrease
the C available to AMF, and thereby suppress AMF growth. Whether
this is the case and could explain the effects of parasitic plants on
SOM decomposition is not known yet.
Here, we tested whether and, if so, how the parasitic plant
Cuscuta australis has a top- down cascading effect on SOM decom-
position via one of its host plants, Bidens pilosa L., and the extraradi-
cal hyphae of an AMF, Rhizophagus intraradices (N.C. Schenck & G.S.
Sm.) C. Walker & A. Schüßler. As the C allocated to the parasitic plant
may reduce the amount of C distributed to the AMF, we hypothe-
sized that the parasitic plant can indirectly regulate SOM decompo-
sition by suppressing the effect of the AMF on decomposition. As
these effects might depend on the type of SOM, we assessed the
effects of the parasitic plant and the AMF on the decomposition of
two types of organic materials, maize leaves and phytate (the most
abundant inositol phosphate in the soil; Turner et al., 2002; Wang
et al., 2017), which have frequently been used in previous studies
testing the effects of AMF on decomposition (Griffiths et al., 2012;
Wang et al., 2013). Our study aimed to unravel the possible mech-
anism by which parasitic plants affect soil nutrient cycling and to
improve our understanding of the ecological roles of parasitic plants
in ecosystems.
2 | MATERIALS AND METHODS
2.1 | Study species
The annual herb Bidens pilosa L. was used as the host plant, and the
herbaceous holoparasite Cuscuta australis R.Br. was used as the par-
asite. Cuscuta australis acquires water, carbon and other nutrients
from its host and can parasitize a wide range of herbaceous species,
including B. pilosa (Li et al., 2015; Zhang et al., 2012). Cuscuta aus-
tralis was chosen because it is an obligate shoot parasite (i.e. has no
roots) and thus cannot have any direct effect on SOM decomposi-
tion. Bidens pilosa was cho sen because it can be parasi tized by C. aus-
tralis, and because it can form symbiosis with AMF (Wei et al., 2012).
2.2 | Substrate, containers and seed germination
The substrate used in our study consisted of a 1:1 mixture of field
soil and sand (v:v). The field soil was sandy, with a pH of 6.69,
12.8 g kg−1 organic matter, 0.648 g kg−1 total N and 0.413 g kg−1
total P, and was obtained from a riverside in the Jiaojiang District ,
Taizhou, China. When collecting field soil, we removed the
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YUAN et a l.
surface soil and collected 120 kg soil from five randomly cho-
sen points within a 10 m2 area. To kill all microbes, all substrate
was autoclaved at 121°C for 2 h. We filled 64 plastic containers
(length × width × height: 20 cm × 10 cm × 11.5 cm) with 1.3 kg
autoclaved substrate each. One plastic core (height × diameter:
8.5 cm × 10 cm), filled with 500 g substrate, was dug into the sub-
strate on one side of each container (Figure S1). The plastic core
had a lateral opening accounting for a quarter of its total surface
area, which was directed toward the other side of the container
(Awaydul et al., 2019). The opening was covered with a 25- μm
nylon mesh that allowed penetration by AMF hyphae but not by
plant roots (Figure S1; Cheng et al., 2012). The plastic core thus
divided the container into separate root+hyphae and hyphae- only
compartments.
After sterilization in 10% sodium hypochlorite, the seeds of B.
pilosa were sown into a plastic plate filled with autoclaved peat, and
placed in a greenhouse on June 12, 2020. On June 27, 2020, when
seedlings of aboveground parts were approximately 2 cm tall (Yuan
et al., 2013), we planted a single seedling of B. pilosa into the plastic
core of each container (Figure S1).
2.3 | Experimental design
We did two experiments that only differed from each other in
the organic material used. Experiment 1 used maize leaves and
Experiment 2 used calcium phytate. Each exp erim ent ha d two fac-
tors: (1) with or without AMF inoculum (+AMF or −AMF); (2) with
or without C. australis parasitization of the host plant (+P or −P).
Each of the four treatment combinations had eight replicate con-
tainers, resulting in 32 containers per experiment, and 64 contain-
ers in total.
For the +AMF treatment, each plastic core received 50 g of AMF
inoculum. The inoculum was derived from pot cultures of Sorghum
bicolor (L.) Moench grown in coarse sand, and consisted of root frag-
ments and soil colonized by the AMF Rhizophagus intraradices, and
its spores. This AMF species was chosen because it is widespread in
natural ecosystems (Moora et al., 2011), and can form symbiosis with
B. pilosa (Zhang, 2015). We mixed the inoculum into the substrate
before seedling transplantation. To correct for possible differences
in microbial communities of the +AMF and −AMF treatments, each
plastic core of the −AMF containers received 50 g of autoclaved in-
oculum and 100 ml of a filtered solution, made from live AMF in-
oculum, and from which AMF spores had been excluded (Cheng
et al., 2012).
Four weeks after transplantation, one 10- cm long stem piece of
C. australis was wound around the stems of the B. pilosa plants to
cause parasitization. This was done in half of the containers, in the
other half we had nonparasitized B. pilosa as controls (Li et al., 20 14).
The stems of C. australis had been collected from a field population
near Taizhou University.
Immediately after addition of the parasite, we buried one
hyphae- in- growth bag (length × width: 6.5 cm × 5.5 cm), made
of 25- μm nylon mesh, into the container at a distance of 7 cm
from the plastic core (Figure S1). For Experiment 1, each bag con-
tained 50 g autoclaved coarse sand and 1.0 g of oven- dried 15 N
and 13C labelled maize leaves. The grain size of the coarse sand
was between 0.425 and 2 mm (Awaydul et al., 2019). The maize
leaves were cut into 1 mm pieces and evenly mixed into the sand.
Because maize is a C4 plant, which naturally has a higher 13C/12C
ratio (δ13C is −13.6‰) than C3 plants (Smith & Epstein, 1971), its
leaves can be treated as being naturally labelled with the 13 C sta-
ble isotope. For 15 N labelling, we had grown the maize plants on
soil supplemented with 15 N - ( N H 4)2SO4 (with 99 atom% of enrich-
ment). For Experiment 2, each bag contained 50 g sand and 0.5 g
calcium phytate (P0410, Tokyo Chemical Industry), which was not
enriched with 13C and 15 N.
To assure that SOM decomposing microorganisms would be
present in the containers, we added, immediately after insertion of
the hyphae- in- growth bags, 50 ml field- soil filtrate to each container.
The filtrate was obtained by adding 250 g of unsterilized field soil to
1 L of sterilized water. This was mixed thoroughly and then passed
through a 38- μm sieve (Xu et al., 2018), which removes the larger
spores and hyphae, such as those of AMF, but allows most other
components of the microbial community to pass (Wagg et al., 2014).
The experiments were conducted in a greenhouse at Taizhou
University, China, with a daily photoperiod of 16 h, and day and
night temperatures of 22°C and 18°C, respectively. Tap water was
sprayed evenly onto the soil of each container every day.
2.4 | Harvest and sample preparation
We harvested the experiments 7 weeks after adding the parasite. All
hyphae- in- growth bags were carefully removed, and 5 g of soil from
each bag was immediately transferred into a −80°C freezer for later
DNA extraction and enzyme- activity measurements. The remaining
soil from each bag was air- dried and then ground to a fine powder in
a ball mill (Retsch Technology GmbH) for nutrient analysis.
The C. australis plants (i.e. the parasites) were harvested by de-
taching them from the B. pilosa host plants. The B. pilosa plant s were
separated into shoots and roots. The plant materials were dried in
a drying oven at 65°C for 72 h and then weighed. After that, the
shoots of B. pilosa were ground into powder by using a ball mill for
analysis of shoot N and P concentrations using the H2SO4- H 2O2
digestion method (Li et al., 20 08). AMF- colonization rate of B. pi-
losa roots was assessed using the gridline- intersection method
(Giovannetti & Mosse, 1980). No AMF colonization was found in the
−AMF treatment.
2.5 | Measurement of 15 N and 13C
In Experiment 1, the 15 N and 13C stable isotope fractions in the hyphae-
in- growth bags and in the shoot of B. pilosa were determined using a
continuous- flow isotope- ratio mass spectrometer (CF- IRMS, Thermo
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YUAN et a l.
Finnigan DELTA Plus). The δ15N (‰) and δ13C (‰) values were con-
verted to absolute isotope ratios (15 N/14 N and 13C/12C). The 15 N and
13C concentrations of the sample were then calculated from fractional
abundances (15 N/[15 N + 14 N] and 13C/[13C + 12C]) and the total N and
C concentration, respectively, of the sample (Cheng et al., 2012; Yuan
et al., 2021). Then, the percentages of 15 N and 13C remaining within the
hyphae- in- growth bags were calculated as the total amounts of N and
C, respectively, in the samples at the end of the experiment divided by
the initial values (i.e. when we added the bags to the containers).
2.6 | Measurements of enzyme activities and
remaining organic P
In Experiment 2, because phytase and acid phosphatase play key roles
in decomposition of phytate (Ding et al., 2014; Wang et al., 2013), we
tested their activities using the soil phytase ELISA kit (Jiangsu Yutong
Biotechnology Co., Ltd) and the soil phosphatase Assay kit (Jiangsu
Yutong Biotechnology Co., Ltd), according to the manufacturer's pro-
tocols. The remaining organic P concentration of the substrate in the
hyphae- in- growth bags was also determined, as it reflects the decom-
position of phytate (Ding et al., 2014). It was calculated by deducting
the inorganic P concentration from the total P concentration (Ding
et al., 2014). The total P concentration in the bags was determined
using a continuous flow analyser, and the inorganic P concentration was
determined using the Olsen method (Jackson, 1973).
2.7 | Analysis of bacterial communities
Three hyphae- in- growth bags per treatment in each experiment (i.e.
24 bags in total) were randomly selected for analysis of the bacterial
communities using the 16 S amplicon- sequencing method (for details,
see Method S1). As measures of microbial alpha diversity, we calcu-
lated the Shannon, Simpson and Pielou's evenness indices. As meas-
ure of beta diversity, we calculated dissimilarities among bacterial
communities by using non- metric multidimensional scaling (NMDS)
at the OTU level based on the unweighted UniFrac distance metric.
In addition, permutational analysis of variance (PERMANOVA) was
used to test for effects of AMF inoculation, parasitization, and their
interaction on bacterial community composition. PERMANOVA was
also used to test for differences in bacterial community composi-
tion between hyphae- in- growth bags with maize leaves and those
with phytate. These analyses were performed in R (version 3.1.2; R
Core Team, 2014, http://www.r- proje ct.org/) using the vegan pack-
age version 3.6 (Oksanen et al., 2011).
2.8 | Statistical analysis
Two- way ANOVAs were used to test the effects of parasitization
and AMF inoculation on the remaining amounts of 15 N, 13 C and or-
ganic P, and on enzyme activities in the hyphae- in- growth bags, as
well as on the growth and nutrient uptake of B. pilosa. We checked
for normality of the residuals using the Shapiro– Wilk test. The
independent- sample t test was used to test the effect of parasiti-
zation on AMF colonization of B. pilosa in +AMF containers (there
was no colonization in the −AMF containers), and the effect of AMF
inoculation on biomass of C. australis. Pearson's correlation analysis
was performed to determine the association between shoot 15 N and
shoot P concentrations in Experiment 1. Pearson's correlation analy-
sis was also performed to determine the associations between acid
phos phatase ac tiv ity in the hyphae - in- grow th bag s and shoot N co n-
centration with shoot P concentration in Experiment 2. Data were
transformed if necessary to improve normality. Specifically, we used
sin- square- root for % 15 N remaining in the hyphae- in- growth bags,
square for AMF colonization rate in Experiment 1, sine for shoot
P content in Experiment 1, and natural logarithm (loge) for shoot P
concentration and for biomass of C. australis in both experiments.
Differences between treatment combinations were compared using
LSD at the 5% significance level. The Shapiro– Wilk tests were run
in R, version 3.5.0 using the shapiro.test function, and all other
analyses were performed using the Statistical Product and Service
Solution (SPSS) software (version 16.0; SPSS Inc.).
3 | RESULTS
3.1 | Effects of the parasite and AMF on
decomposition and enzymatic activities
In Experiment 1 (with maize leaves), the percentage of 15 N remain-
ing in the hyphae- in- growth bags was not significantly affected by
parasitization and AMF inoculation (Table 1; Figure 1a). However,
the percentage of 13C remaining in the bags was significantly lower
in the +AMF/−P treatment combination than in the other three
treatment combinations (significant AMF × parasitism interaction in
Table 1; F1,26 = 6.373, P = 0.018; Figure 1b).
In Experiment 2 (with phytate), the organic P remaining in the
hyphae- in- growth bags was higher in the +AMF than in the −AMF
treatment, and higher in the −P than in the +P treatment (Table 1;
Figure 1c). Although the effect of the AMF treatment was stronger
for −P than for +P (Figure 1c), the AMF × parasitism interaction was
not statistically significant (Table 1). Furthermore, AMF inoculation
significantly decreased the phytase activity, whereas parasitization
did not (Figure 1d). Parasitization tended to slightly increase the acid
phosphatase activity, although this effect was only visible for +AMF
(Table 1; Figure 1e).
3.2 | Effects of parasite on AMF- colonization
rates of Bidens pilosa
Parasitization significantly decreased the AMF- colonization rate of
B. pilosa in Experiment 1 (t = 2. 519, P = 0.025; Figure 2a), but not in
Experiment 2 (t = 1.084, p = 0.297; Figure 2b).
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YUAN et a l.
3.3 | Effects of the parasite and AMF on bacterial
communities
In Experiment 1, a total of 1,258,474 16 S reads, belonging to 27
bacterial phyla, were detected. The bacterial communities were
dominated by the phyla Firmicutes (~50%), Proteobacteria (~29%),
and Actinobacteria (~12%; Figure S2a; Table S1), and by the genera
Bacillus (~36%), Devosia (~3%) and Pseudomonas (~2%; Figure S3a;
Table S3). In the presence of AMF, parasitization significantly
increased the abundance of the phylum Gemmatimonadetes
(F1,4 = 8.65, p = 0.042; Table S1). Most of the dominant bac-
terial genera did not show significant dif ferences among the
treatment combinations, with the exception that for +AMF, parasiti-
zation significantly increased the abundance of Bacillus (F1,4 = 22.24,
P = 0.009; Table S3). Furthermore, AMF inoculation significantly
decreased the abundance of the genus Paenibacillus (F1,10 = 10.52;
P = 0.009; Table S3). For the three measures of alpha diversity of
the bacterial communities, there was only a significant effect for the
Simpson index: parasitization significantly decreased it for +AMF
(F1,4 = 34.26; P = 0.0 04; Figure S4c). PERMANOVA showed that the
bacterial community composition was not significantly affected by
AMF inoculation (r2 = 0.101, p = 0.234), parasitization (r2 = 0.072,
p = 0.937) and their interaction (r2 = 0.109, p = 0.143; Figure 3a).
In Experiment 2, a total of 1,209,931 16 S reads, belonging to 32
bacter ia l phy l a , we r e de t e c ted. Th e ba c terial communitie s we r e do m -
inated by the phyla Proteobacteria (~44%), Actinobacteria (~26%)
and Firmicutes (~12%; Figure S2b; Table S2), and by the genera TRA3-
20 (~4%), Pseudomonas (~4%) and Streptomyces (~3%; Figure S3b;
Table S4). AMF inoculation significantly decreased the abundance
of the dominant phyla Firmicutes (F1,10 = 8 .77; p = 0.014; Table S2)
and Cyanobacteria (F1,10 = 5.12; p = 0.047; Table S2). Most bacterial
genera did not show significant differences among the treatment
combinations, except for +AMF, where parasitization significantly
decreased the abundance of the genus Streptomyces (F1,4 = 28.07;
p = 0.006; Table S4). The alpha diversity of the bacterial community
was not significantly affected by AMF inoculation and parasitization
(Figure S4). PERMANOVA showed that the bacterial composition
was sign ificantl y affected by AMF inoc ulation (r2 = 0.118 , p = 0.038),
but not by parasitization (r2 = 0.082, p = 0.643) and their interaction
(r2 = 0.085, p = 0.590; Figure 3b).
3.4 | Effects on growth and nutrient uptake of
Bidens pilosa and Cuscuta australis
In both experiments, parasitization significantly decreased bio-
mass of B. pilosa, but this effect was only significant for +AMF
(Figure S6a,c). The root weight ratio of B. pilosa tended to be lower
for parasitized plants, but this effect was not statistically significant
(Figure S6b,d). In both experiments, AMF inoculation did not signifi-
cantly af fect biomass of C. australis (Figure S7).
In Experiment 1, parasitization significantly increased shoot 15 N
concentration of B. pilosa, but this was only statistically significant
for +AMF (Figure 4a). Moreover, for +AMF, shoot 15 N and P concen-
tration of B. pilosa was significantly positively correlated (Figure 4b),
suggesting that the uptake of both nutrients was linked.
TAB LE 1 Effects of AMF inoculation and parasitization by Cuscuta australis on 15 N and 13 C remaining in hyphae- in- growth bags, on 15 N
uptake by Bidens pilosa in Experiment 1, and on the organic P remaining and the activities of the enzymes phytase and acid phosphatase in
the hyphae- in- growth bags in Experiment 2. Significant differences (p < 0.05) are marked in bold
Variables Source of variation df F p
Experiment 1 15 N remaining AMF 1, 26 2.152 0.154
parasitism 1, 26 1.301 0.264
AMF × parasitism 1, 26 0.728 0.401
13C remaining AMF 1, 26 0.862 0.362
parasitism 1, 26 1.933 0.176
AMF × parasitism 1, 26 6.373 0.018
Shoot 15 N concentration AMF 1, 28 0.484 0.492
parasitism 1, 28 7.62 0 0.010
AMF × parasitism 1, 28 2.694 0.112
Experiment 2 Organic P remaining AMF 1, 25 4.428 0.046
parasitism 1, 25 4.767 0.039
AMF × parasitism 1, 25 1.282 0.268
Phytase activity AMF 1, 28 9.70 9 0.004
parasitism 1, 28 <0.001 0.995
AMF × parasitism 1, 28 0.005 0.945
Phosphatase activity AMF 1, 28 0.939 0.3 41
parasitism 1, 28 2.990 0.095
AMF × parasitism 1, 28 1. 520 0.228
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YUAN et a l.
In Experiment 2, the acid phosphatase activity in hyphae- in-
growth bags was significantly positively correlated with the shoot P
concentration of B. pilosa for +AMF (Figure 4c). For +AMF, the shoot
N concentration of B. pilosa was significantly positively correlated
with the shoot P concentration (Figure 4d).
4 | DISCUSSION
The results of our two experiments (summarized in Figure 5) pro-
vide insights into the cascading effects of parasitic plants on SOM
decomposition and soil- nutrient cycling. We found that the parasite
decreased the decomposition of maize leaves and increased the
decomposition of phytate, but only in the presence of AMF. We
also found that AMF increased the decomposition of maize leaves,
whereas it decreased the decomposition of phytate, but only in the
absence of the parasite. So, the parasite neutralized the effect of the
AMF on SOM decomposition. In other words, the results support
our hypothesis that parasitic plants can indirectly regulate SOM dy-
namics by suppressing the effect of AMF on decomposition.
Changes in the amounts of organic material remaining in the
hyphae- in- growth bags in the two experiments suggest that AMF
FIGURE 1 Organic materials remaining in the hyphae- in- growth bags and enzyme activities. 15 N (a) and 13C (b) remaining in the bags
of Experiment 1, and organic P remaining (c), phytase activity (d), and acid phosphatase (Pase) activity (e) in the bags of Experiment 2. −P:
Bidens pilosa not parasitized by Cuscuta australis; +P: B. pilosa parasitized by C. australis; −AMF: without AMF inoculation; +AMF: with AMF
inoculation. Values are means ± SE. Different lowercase letters indicated a significant difference (p < 0.05) between treatment combinations.
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YUAN et a l.
had opposite effects on the decomposition of maize leaves and phy-
tate. The reason for this could be differences in nutrient release from
these two organic materials, especially the P availability (Figures S5
and S10). It has been shown that nutrient release from SOM can
directly shape the microbial community (Abril et al., 2021; Ferreira
& Graça, 2016). However, the presence of AMF may have further
changed the composition of the microbial communities or the activ-
ities of the microbial decomposers, and therefore the final decom-
position of maize leaves and phytate by AMF after 2 months may
have been different, or even opposite. On the other hand, it could
be that the nutrients released from maize leaves and phytate may
affect competition between AMF and the bacterial decomposers
differently. Previous studies have shown that high soil- P availabil-
ity can exacerbate N competition between AMF and decomposers
(Jannoura et al., 2012; Xu et al., 2018). When P availability is rela-
tively low (i.e. when there is a high N:P ratio), AMF may promote
decomposition, whereas under high soil- P availability— as would re-
sult from decomposition of phytate— AMF may suppress the decom-
position of organic matter (Xu et al., 2018). Therefore, we speculate
that the high P availability in the hyphae- in- growth bags with phy-
tate may make the bacterial decomposers suffer from stronger N
competition with AMF, and this may reduce the bacterial production
of the enzyme phytase. Consequently, AMF was more likely to pro-
mote the decomposition of maize leaves, whereas the opposite was
true for phytate. However, how the bacterial community and nutri-
ents released from maize leaves and phytate differently affect the
relationship between AMF and SOM decomposition needs further
stud y.
Irrespective of the opposing AMF effects on decomposition of
the two organic materials, the presence of the parasite suppressed
or offset the effect of AMF on decomposition. A reason for this
could be that the parasite decreased C allocation from the host to
AMF (Sui et al., 2019). This is supported by our finding that para-
sitization decreased AMF colonization of B. pilosa (Figure 2), most
likely as a consequence of competition for C. Although AMF provide
N and P to the host plant, they rely, just like the holoparasite, for
C on the host. It has been estimated that 10%– 23% of the photo-
synthates of the host can be transferred to their AMF (Jakobsen &
FIGURE 2 AMF- colonization rate of Bidens pilosa in Experiment 1 (a) and Experiment 2 (b). −P: B. pilosa not parasitized by Cuscuta
australis; +P: B. pilosa parasitized by C. australis. Values are means ± SE. *Indicates that means are significantly different; ns indicates that
means are not significantly different.
FIGURE 3 Differences in composition of the bacterial communities in the hyphae- in- growth bags are shown as Nonmetric
Multidimensional Scaling (NMDS) plots for Experiment 1 (a) and Experiment 2 (b). −AMF/−P: without AMF inoculation and without parasite;
−AMF/+P: without AMF inoculation and with parasite; +AMF/−P: with AMF inoculation and without parasite; +AMF/+P: with AMF
inoculation and with parasite.
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8
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Functional Ecology
YUAN et a l.
Rosendahl, 1990 ; Kucey & Paul, 1982). Direct competition for C be-
tween AMF and the parasite may thus have limited AMF growth and
thereby suppressed the effect of AMF on decomposition (Figure 5).
Another possible explanation for the suppressive effect of the para-
site on the effect of AMF could be that parasitization of the host plant
changed the chemicals (like secondary metabolites, hormonome) re-
leased from its roots (Mishev et al., 2021; Shen et al., 2020), and that
this influenced AMF growth. For example, parasitization of plants by
Phelipanche spp. led to the changes in the production of cytokinins,
which can influence AMF development (Mishev et al., 2021; Pons
et al., 2020). However, which mechanism plays the main role needs
further testing. It should also be noted that our result s are only a
snapshot after 2 months of plant growth. Therefore, whether the ef-
fects of parasitization and AMF on decomposition changes with time
needs further study.
AMF have been considered to affect SOM decomposition
by influencing the bacterial community (Nuccio et al., 2013; Xu
et al., 2018). We found that AMF inoculation significantly af fe cted
the bacterial community in the hyphae- in- growth bags with phy-
tate (Experiment 2). Because AMF have no known saprotrophic
capability, that is they lack the ability to secrete enzymes like
phosphatases (Tisserant et al., 2013; Zhang, Cao, et al., 2016), it
is likely that changes in the bacterial community caused by AMF
altered the secretion of enzymes by microbial decomposers, which
then changed the decomposition of phytate. Interestingly, AMF
inoculation did not significantly affect the diversity and composi-
tion of the bac ter ial comm unity in th e hyphae- in - gr owth bags with
maize leaves. Nevertheless, AMF significantly affected the abun-
dance of some genera, like Paenibacillus (Figure S2). As studies
have shown that Paenibacillus are associated with AMF and com-
ponents of the soil- nutrient cycle, like nitrogen fixation and phos-
phorus solubilization (Coelho et al., 2003; Larsen et al., 2009), it is
likely that the decreased abundance of the genus Paenibacillus may
affect decomposition.
Parasitization of B. pilosa by C. australis did not significantly
change the composition of the bacterial community in both ex-
periments. Nevertheless, parasitization decreased the Simpson
diversity index and increased the abundance of the genus Bacillus
in Experiment 1, and decreased the abundance of the genus
Streptomyces in Experiment 2. Previous work has shown that
FIGURE 4 The shoot 15 N concentration (a), and the correlation between shoot 15 N concentration and shoot P concentration in the
presence of AMF (b) in Experiment 1. And the correlation between acid phosphatase activity in the hyphae- in- growth bags and shoot P
concentration of B. pilosa (c), and the correlation between shoot N concentration and shoot P concentration (d) in the presence of AMF in
Experiment 2. −P: Bidens pilosa not parasitized by Cuscuta australis; +P: B. pilosa parasitized by C. australis. −AMF: without AMF inoculation;
+AMF: with AMF inoculation. Values are means ± SE. Different lowercase letters indicated a significant difference (p < 0.05) between
treatment combinations.
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Functional Ecology
YUAN et a l.
both Bacillus and Streptomyces are associated with decomposition
(Chater, 1993; Nalini et al., 2020; Nuccio et al., 2013). In particular,
Bacillus species have been shown to be associated with decompos-
ing hyphae (Artursson & Jansson, 2003; Toljander et al., 2006), while
Streptomyces and other Actinobacteria have been shown to be major
contributors to biological buffering of soils and play important roles
in SOM decomposition (Chater, 1993; Nalini et al., 2020). Therefore,
the effect of the parasite on these groups may be relevant for de-
composition. Although more studies are needed to test the role of
the bacterial community in SOM decomposition, our results indicate
that the genera Bacillus and Streptomyces are involved in the regula-
tion of the decomposition by AMF and the parasitic plant.
Based on the different characteristics of maize leaves and phy-
tate, we measured different variables in the two experiments to
evaluate the effect of the parasite and AMF on decomposition and
on nutrient uptake by AMF hyphae. In Experiment 1, we used the
amounts of 13C and 15 N remaining in the hyphae- in- growth bags
to quantify the amount of SOM that had been decomposed. This
approach has also been used in previous studies (Qiu et al., 2016;
Verbruggen et al., 2016; Xu et al., 2018). We found that the 13C re-
maining in the hyphae- in- growth bags was significantly affected by
AMF and the parasite, but that the 15 N remaining in the bags was
unaffected. This is similar to the results of a study by Verbruggen
et al. (2016) showing that AMF hypha increased 13 C loss in hyphae-
in- growth cores, whereas 15 N content was unaffected. Both the
result s of Verbr uggen et al. (2016) and our results indicate that litter-
derived 13C was lost as CO2 from the soil. This indicates that 13 C may
be a better indicator for decomposition than 15 N, because the 13CO2
that is produced in decomposition is removed whereas the inorganic
15 N that is produced might remain in the soil.
In Experiment 2, as the activities of phytase and acid phospha-
tase have been reported to be correlated with the decomposition of
phytate (Ding et al., 2014; Wang et al., 2013), we tested their activi-
ties to assess the effect of the parasite and AMF on decomposition.
We found that AMF, but not the parasite, significantly decreased
phytase activity, while the parasite, but not AMF, significantly in-
creased the acid phosphatase activity. These results indicate that
the parasite did not simply reduce the effect of AMF on the activity
of phytase, but may induce a new pathway via AMF to change the
activity of acid phosphatase to regulate SOM decomposition.
Previous studies have shown that the effect of AMF on SOM
decomposition sometimes affects (Xu et al., 2018) and sometimes
does not affect (Hodge et al., 2001) the uptake of nutrients re-
leased from organic matter. Our 15 N tracing results showed that
the decomposition of maize leaves did not increase the N uptake by
B. pilosa (Figure 4a). However, the significant correlation between
shoot P concentration and acid phosphatase activity in the hyphae-
in- growth bags showed that the decomposition of organic P may
increase P uptake from decomposed organic matter (Figure 4c). As
in both experiments shoot N and P concentrations were positively
FIGURE 5 A conceptual framework of the cascading effect of parasitic plants on the decomposition of soil organic matter (SOM) via
extraradical hyphae of AMF. Overall, the parasitic plant directly suppressed the host plant growth, which in turn indirectly suppressed AMF
growth. The characteristics of SOM modified the composition of the decomposing bacteria or differently changed the physicochemical
environment for decomposers. This drove the AMF to change their influence on the decomposing bacteria, which then promoted or
suppressed decomposition. Therefore, the presence of the parasite either indirectly decreased SOM decomposition (like found for maize
leaves in Experiment 1) or increased SOM decomposition (like found for phytate in Experiment 2). Solid and dashed lines indicate direct
and indirect effects, respectively. Red and light blue arrows, accompanied by + and – symbols, indicate positive and negative effects,
respectively. Black arrows, accompanied by a circular arrows symbol, indicate a change in the bacterial community (which cannot be
quantified as positive or negative). The dark blue dashed line with a T- heading indicates that the presence of the parasite neutralized the
effect of AMF on SOM. The numbers of the figures that show the indicated effects are given in grey font. *: the positive effect of the host
plant on the parasite and AMF is given, †: the negative effect of decomposing bacteria on SOM is given.
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10
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Functional Ecology
YUAN et a l.
correlated (Figure 4b,d), it is likely that the N and P uptake of host
plants was jointly regulated by plant intrinsic properties. This might
be, because host plants need to maintain a certain N:P stoichiomet-
ric balance to function properly (Fujita et al., 2 010).
Soil organic C decomposition can also be affected by other fac-
tors than AMF, such as by soil nutrient availability, soil moisture con-
tent and detritivore activity (Ge et al., 2018; Tonin et al., 2018; Xu
et al., 2018). For example, Ge et al. (2018) found that drought de-
creased carbon storage in the upper 60 cm of the soil by 12.2%. Xu
et al. (2018) found that without AMF, the 13C remaining in litter bags
was ~5% lower at high than at low soil P concentration, whereas with
AMF, the 13C remaining in litter bags was ~6% higher at high than at
low soil P concentration. In our experiments, AMF decreased the
13C remaining in the hyphae- in- growth bags by ~31% in the absence
of the parasite, whereas it increased the remaining 13 C remaining
by ~16% in the presence of the parasite. So, the magnitude of the
effect of AMF on SOM decomposition appears to be higher than the
effects of other factors, which indicates the important role of AMF
in soil nutrient cycling.
In this study, we only used one AMF species (R. intraradices), one
parasitic plant species (C. australis), one host plant species (B. pilosa)
and one field soil location. This means that the results cannot be
generalized yet. However, as R. intraradices is a widespread AMF
species (Moora et al., 2011), which has been used as a representative
AMF species in many studies (Rodriguez- Caballero et al., 2017; Wu
et al., 2015), it is highly likely that R. intraradices is one of the main
AMF species through which C . australis and other parasites can in-
directly affect SOM decomposition in the field. Furthermore, based
on the observed intermediate growth of the host plants, we judge
that the field soil we had collected was neither extremely nutrient-
rich nor extremely nutrient- poor, and thus representative for many
soils. Although we c annot yet generalize our findings, we believe
our study paves the way for further studies with more AMF species,
plant species and field soil origins.
The roles of different plant species and functional groups in de-
termining ecosystem processes is a major focus of ecology. Parasitic
plants are one group of plants which are known to influence soil nutri-
ent cycling, but the mechanism has rarely been explored. Our results
show for the first time that a parasitic plant can indirectly regulate
SOM decomposition by suppressing the effect of AMF on decompo-
sition (Figure 5). Our study provides an example of how a parasitic
plant can trigger a series of cascading effects between above- and
belowground processes. Such trophic cascades have been frequently
reported in studies on herbivory (van Dam & Heil, 2011; Zhuang
et al., 2018), but less so in studies on parasitic plants. Our results high-
light the importance of cascading effects in a community context to
unravel the mechanisms underlying sophisticated hidden ecological
processes, and represents an important step forward in elucidating
the roles of parasitic plants in soil nutrient cycling. Our study indicates
that future work needs to take AMF into account when exploring the
mechanisms that underly the effect of parasitic plants on SOM de-
composition, and more work is needed to test the interactions of mi-
crobial decomposers with AMF and with parasitic plants.
AUTHOR CONTRIBUTIONS
Yongge Yuan and Junmin Li conceived the ideas and designed the
experiments. Yongge Yuan, Xinru Lin, and Gelv Chen performed the
experiments. Junmin Li and Yongge Yuan analysed the data. Junmin
Li and Yongge Yuan prepared the manuscript. Junmin Li, Yongge Yuan
and Mark van Kleunen improved the manuscript. All authors contrib-
uted critically to the drafts and gave final approval for publication.
ACKNOWLEDGEMENTS
This study was suppor ted by the Zhejiang Provincial Natural
Science Foundation (LY21C030004), the National Natural Science
Foundation of China (32271630, 32271590, 31500416), the
Outstanding Youth Fund of Taizhou University (2019YQ002), the
211 Talent Training Fund of Taizhou (2018), and the Ten Thousand
Talent Program of Zhejiang Province (2019R52043).
CONFLICT OF INTEREST
The authors have no conflict of interest.
DATA AVA ILAB ILITY STATE MEN T
Data are available from the Figshare https://doi.org/10.6084/
m9.figsh are.21366186
ORCID
Yongge Yuan https://orcid.org/0000-0002-4949-7498
Junmin Li https://orcid.org/0000-0001-8244-0461
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