1. Introduction
Plant competition refers to the interrelationships between plants when the required environmental resources or space are relatively insufficient [
1]. Competitiveness is a key factor that determines whether exotic plants successfully invade new environments [
2]. When strongly competitive exotic plants compete for resources with invasive species, they can successfully exclude local plants, greatly reducing the biodiversity of the invasive area and disrupting the ecological balance [
3]. Therefore, studying the competitiveness of exotic plants has become a hot topic in invasion ecology.
Parasitic plants, as local natural enemies, play an important regulatory role in alien plant populations and a decisive role in the invasion process of alien plants [
4], and are important natural enemies that absorb water and nutrients from their host plants (e.g., invasive plants such as
Solidago canadensi L. and
Alternanthera philoxeroides (Mart.) Griseb.) through suckers. Simultaneously, because the photosynthesis of the host plant is affected, its growth inhibition exceeds the accumulation of its biomass, affecting its growth, development, and competitiveness [
5,
6].
Hypotheses related to exotic plants and their natural enemies include the enemy release hypothesis, biotic resistance from enemies hypothesis, evolution of increased competitive ability hypothesis, evolutionary reduced competitive ability hypothesis, biotic resistance from competitors hypothesis, and the new association hypothesis of competitive objects. Enemy release and biotic resistance from enemies suggest that when invading plants enter a new environment, local or exotic natural enemies may prevent the invasion of exotic plants through predation or parasitism or alleviate the invasion pressure by inhibiting or delaying settlement [
7,
8,
9]. The evolution of increased competitive ability suggests that exotic plants in their native areas need to invest certain resources for defense owing to the influence of natural enemies, which can affect their growth and reproduction. In invasive areas, due to the lack of natural enemies, resources originally used for defense can be used for growth and reproduction, improving their competitiveness [
10,
11,
12]. The evolutionarily reduced competitive ability suggests that if there is less competition in invasive areas and competition involves adaptive cost characteristics, invasive species may evolve in a direction that has adverse effects on them, reducing intraspecies interactions [
13,
14]. The biotic resistance of competitors suggests that in new environments, exotic plants compete with local or other exotic plants to prevent their invasion by inhibiting their settlement, domestication, and persistence through competition for nutrients, water, light, and other resources [
15,
16]. These new associations suggest that invasive species form new relationships with other species in the community, and the impact of this relationship on alien plants usually manifests as promoting or preventing the successful invasion of new habitats by alien plants.
According to field investigations in the suburbs of Urumqi, Xinjiang,
Cuscuta australis can effectively parasitize two invasive plants in the composite family,
Xanthium spinosum and
Xanthium italicum.
X. spinosum is an invasive weed native to South America [
17]. This species has a strong growth and reproduction ability, high seed yield, and numerous dispersal media, and can quickly occupy a large area, inhibiting the growth and reproduction of local plants and crops [
18]. The entire plant has slight toxicity and many sharp yellow thorns in its long petiole; thus, cattle and sheep do not feed on this plant, which directly or indirectly affects the development of agriculture and animal husbandry in the invaded area [
19].
X. italicum, an annual invasive weed, is native to North America [
20]. This species has a well-developed root system, strong ecological adaptability, large growth capacity, high seed-setting rate, wide seed transmission pathways, and seeds with thorns, which seriously affect the local ecological environment, animal husbandry, and agriculture [
21].
C. australis is a parasitic plant of
Cuscuta spp. in the family Convolvulaceae [
22] and is recognized as a harmful weed in agriculture and forestry [
23,
24].
With the increasing severity of global biological invasions, the use of local parasitic plants to prevent and control exotic plants, known as “grass control”, has become a research hotspot. Moreover, studying the relationship between
C. australis and two invasive species of
Xanthium would provide a theoretical basis for the biological control of these two invasive species. Studies have shown that plants belonging to the genus
Cuscuta effectively inhibit the growth of invasive plants and restore local communities. For example, parasitism by
C. australis significantly reduces the net assimilation rate (NAR) and relative growth rate (RGR) of
Bidens pilosa L. [
25], and parasitism by
C. australis of
A. philoxeroides can significantly increase its root-to-shoot ratio and community diversity, promoting the recovery of local communities [
26].
Based on field observations and the literature, we hypothesized that parasitism by C. australis would affect the biomass allocation and competitiveness of X. spinosum and X. italicum. However, no relevant reports have investigated the impact of the parasitism of C. australis on the competitive ability of the two species of Xanthium. Therefore, in this study, we focus on the changes in the biomass, allocation, and competitiveness of X. spinosum, X. italicum, and C. australis during their parasitism, seedling parasitism, flowering parasitism, and fruiting parasitism.
The aim was to understand the parasitic relationship between C. australis, X. spinosum, and X. italicum; evaluate whether parasitic plants can become effective biological control agents to provide a theoretical basis for the biological control of invasive plants; and answer three scientific questions, namely: (1) How does the biomass of X. spinosum and X. italicum parasitizing C. australis in southern China change? (to verify the growth-defense trade-off and resource availability hypothesis); (2) How does the parasitism of C. australis affect the relative intensity of competition between X. spinosum and X. italicum? (to verify the evolution of the increased competitive ability and the evolutionary reduced competitive ability hypothesis); and (3) What is the effect of parasitism of C. australis on the growth cycles of X. spinosum and X. italicum?
2. Materials and Methods
Seed collection:
C. australis,
X. spinosum, and
X. italicum were the experimental materials collected from dry plants from March to April 2021. Seeds of
C. australis were collected from plants near the Sanping Farm in Urumqi. Seeds of
X. spinosum and
X. italicum were collected from dry plants along the forest belt and roads of Sanping Farm in Urumqi. (
Table 1) For seed collection, 50 plants were randomly selected from each natural population, and from three to five fruits were collected from each plant. Seeds collected from all
X. spinosum plants were mixed. Similarly, the seeds collected from all selected
X. italicum plants were mixed. The normally developing seeds were placed in labeled envelopes and stored in a refrigerator at 4 °C for the subsequent potted experiments.
2.1. Study Area
The experiment was conducted at the Sanping Teaching and Internship Base of Xinjiang Agricultural University. The geographical coordinates were 43°56′ N, 87°20′ E, and the altitude was 790 m. The site was on an alluvial plain on the southern edge of the Junggar Basin, which has a typical continental temperate desert climate: hot and dry in the summer and cold in the winter. The average annual temperature was 7.2 °C, the average annual precipitation was 194.3 mm, and the soil was desert clay.
2.2. Experimental Design
In May 2021, the three plant seeds were placed in degradation bags containing built-in labels. The bags were buried in a storage box containing sterilized sand moistened with distilled water. The seeds were then subjected to low-temperature stratification treatment at 4 °C for 2 weeks to improve the germination rate of southern dodder and two types of xanthium seeds [
27].
(1) Competitive ability: The samples were divided into two groups, single species and mixed species, based on Feng [
27]. One plant was placed in each flowerpot for a single species, and two plants of the same species were placed in each flowerpot for the mixed species (one plant was not treated, and the other plant was treated at different stages of parasitism). Each plant was treated using four treatments: not parasitism (control group), seedling parasitism, flowering parasitism, and fruiting parasitism. Each treatment had 10 replicates; thus, there were 160 flowerpots. For the parasitic treatment group in the seedling stage, the seeds of
C. australis were sowed at a distance of 5 cm from the target plant seeds 5 d after sowing to ensure that the target plant emerged earlier than
C. australis. After the emergence of
C. australis, one successful parasitic plant of
C. australis was retained, and the excess
C. australis was removed. For the flowering parasitism treatment group, the seeds of
C. australis were sowed at a distance of 5 cm from the target plant when the target plant began to bud, ensuring that
C. australis could successfully parasitize when the target plant reached flowering. After
C. australis emerged, one successfully parasitized
C. australis plant was retained, and the excess plants were removed. During the fruit stage, when the flowers of the target plant began to shed, the
C. australis was sown 5 cm from the target plant. After
C. australis emerged, a successfully parasitized
C. australis plant was retained, and additional plants were removed. Mixed planting involved the parasitic treatment of only one plant in the pot.
(2) Phenology (Growth time): The plants were divided into treatment and control groups by using a single planting method (
Figure 1). The treatment group received the parasitic treatment with
C. australis, and the control group did not receive parasitical treatment with
C. australis (
Figure 1). From three to five seeds of the three types of plants were sown into flowerpots, and 5 d after sowing, from three to five seeds of
C. australis were sown into flowerpots in the treatment group, 5 cm from the plants. After the target plant and
C. australis emerged, one target plant with consistent growth in each flowerpot and one successfully parasitized
C. australis were retained, and excess plants were removed.
Starting from the emergence of X. spinosum and X. italicum, the emergence time, bud emergence time, flowering time, fruiting time, and fruit ripening time of the X. spinosum and X. italicum treatment and control groups were recorded.
(3) Collection and measurement: After the fruits of X. spinosum and X. italicum matured, each planting plant was separated into the root, stem, leaf, and fruit and placed in a brown paper bag with corresponding labels. After being transported to the laboratory, they were blanched at 105 °C for 20 min and dried at 70 °C to constant weight. The biomass of each component of the three invasive plants was measured using a percentile electronic balance with an accuracy of 0.01 (J-SKY).
(4) Data analysis: Excel was used for preliminary data integration. SPSS 26.0, one-way ANOVA, and Origin 2018 were used for thedata analysis.
Pmono represents the average value of the plant height, crown width, or biomass for a single species, and Pmix represents the corresponding value of each indicator for the mixed species.
3. Results
The total and aboveground biomass of
X. spinosum parasitized during the flowering and fruiting stages of
C.
australis increased by 48%, 10%, 47%, and 12%, respectively. The difference between
X. spinosum and the plants without parasitization was significant, with a decrease of 22% and 25%, respectively (
p < 0.05). The root biomass increased by 65% during parasitism during flowering, significantly higher than the increase under not parasitism (2%). The stem biomass increased by 26% and 14% during flowering and fruit parasitism, respectively, a significant difference from a decrease of 29% without parasitism (
p < 0.05). The fruit biomass increased by 33% under parasitism during flowering and decreased by 38% under not parasitism, indicating a significant difference (
p < 0.05). The increase in plant height during parasitism during the flowering and fruit stages was significantly higher than that of not parasitism. The total biomass and aboveground biomass of
X. italicum parasitized during the seedling and flowering stages of
C. australis decreased by 56%, 62%, and 54%, and 63%, significantly higher than the not parasitized reduction value (
p < 0.05). The root biomass decreased by 61%, 54%, and 5% during the seedling, flowering, and fruit stages, respectively, with a significant difference from the 26% increase without parasitism (
p < 0.05). The stem biomass decreased by 59%, 64%, and 6% during the seedling, flowering, and fruit stages, respectively, with a significant difference from an increase of 30% without parasitism (
p < 0.05). The leaf biomass decreased by 54% and 59% during parasitism during the seedling and flowering stages, respectively, significantly higher than the decrease in not parasitism (6%) (
p < 0.05). The parasitic reduction of fruit biomass by 60% during flowering was significantly higher than the not parasitic reduction value (12%) (
p < 0.05). These results demonstrate that compared with that of the control, the parasitism of
C. australis at different stages significantly increased the biomass of
X. spinosum and significantly decreased the biomass of
X. italicum (
Figure 2).
Parasitism by
C. australis significantly affected the biomass allocation of
X. spinosum and
X. italicum. Compared with that of the control, the root-to-shoot ratio of
X. spinosum significantly increased during seedling parasitism; the leaf biomass ratio significantly increased during flowering parasitism; and the stem biomass ratio significantly increased during seedling, flowering, and fruit parasitism. The fruit biomass ratio significantly decreased during seedling, flowering, and fruit parasitism (
p < 0.05). The root-to-shoot ratio and stem biomass ratio of
X. italicum significantly increased during parasitism at the seedling, flowering, and fruit stages. The leaf biomass ratio significantly increased during parasitism at the seedling and flowering stages. The fruit biomass ratio decreased significantly during parasitism at the seedling, flowering, and fruit stages (
p < 0.05). The results demonstrate that parasitism by
C. australis caused
X. spinosum and
X. italicum to change their biomass allocation strategies, increasing the energy required for nutrient growth and decreasing the energy input for reproductive growth (
Figure 3).
Under mixed planting conditions,
X. spinosum parasitized
C. australis during the flowering and fruit stages, with negative RCI values calculated based on both the individual aboveground biomass and total biomass, which were significantly less than zero (
p < 0.05) under parasitized conditions during the flowering and fruit stages. The RCI of individual total biomass parasitized during the flowering and fruit stages was significantly lower than that under the not parasitized condition and seedling stages. The parasitism of
C. australis during the flowering and fruit stages enhanced the competitive ability of
X. spinosum. The RCI of
X. italicum, calculated based on the root, aboveground, and total biomasses of a single plant, was positive and significantly greater than 0 (
p < 0.05) during the parasitism of
C. australis during the seedling and flowering stages, indicating that parasitism by
C. australis during the seedling and flowering stages reduced the competitiveness of
X. italicum (
Table 2).
The parasitism of
C. australis shortened the growth cycles of the two invasive weeds (
Figure 4). Compared with the control, the growth period of
X. italicum was shortened by 10 d, the fruiting period by 4 DAS, the growth period of
X. spinosum by 9 DAS, and the fruiting period by 3 DAS. The growth periods of
X. italicum and
X. spinosum were significantly shortened, and the fruiting periods of both invasive weeds were significantly shortened.
Compared with that of the control, the parasitism of
C. australis significantly advanced the budding time of
X. spinosum and
X. italicum by approximately 9 and 8 DAS, respectively. For flowering, the parasitism of
C. australis significantly advanced the flowering time of
X. spinosum by approximately 8 DAS and that of
X. italicum by approximately 7 DAS. For fruiting, the parasitism of
C. australis significantly advanced the fruiting time of
X. spinosum by approximately 10 DAS and that of
X. italicum by approximately 9 DAS. In addition, the parasitism of
C. australis significantly advanced the fruit ripening time of
X. spinosum and
X. italicum, respectively, by approximately 13 and 12 DAS (
Figure 5). These results demonstrate that the parasitism of
C. australis not only shortened the growth cycle of the two invasive weeds, but also advanced them.
The parasitism of
C. australis not only accelerated and shortened the life cycle of
X. spinosum and
X. italicum, but also changed the biomass and plant height indicators of the two invasive weeds. The total biomass, fruit biomass, plant height, and crown width of
X. spinosum parasitized by
C. australis decreased by 88%, 92%, 54%, and 70%, respectively; the total biomass, fruit biomass, plant height, and crown diameter of
X. italicum decreased by 96%, 99%, 79%, and 71%, respectively, significantly different from those without parasitism (
Figure 6). Thus, under the parasitism of
C. australis,
X. spinosum and
X. italicum not only advanced their life cycle, but also inhibited their biomass, plant height, and crown width.
4. Discussion
C. australis had the greatest impact on plant growth and flowering when parasitized, increasing the biomass of X. spinosum by 48% and reducing the biomass of X. italicum by 62% compared with those of the not parasitized plants; it also increased the root-to-shoot ratio and decreased the fruit biomass ratio of X. spinosum and X. italicum, indicating that the parasitism of C. australis changed the growth and reproduction strategies of X. spinosum and X. italicum. By calculating the relative competitive intensity (RCI), the parasitism of C. australis enhanced the competitive ability of X. spinosum, and the competitive ability of X. italicum decreased. The parasitism of C. australis extended the growth period of X. spinosum by 9 d and the growth period of X. italicum by 10 d. This result indicates that although parasitism by C. australis enhanced the competitiveness of X. spinosum, it had an inhibitory effect on the growth of X. spinosum and X. italicum, which had a significant impact on the reproduction and diffusion of X. spinosum and X. italicum in invasive areas.
Often, biomass is an important parameter for measuring plant invasiveness, and a high biomass often leads to a strong reproductive ability and high fitness [
28,
29]. Additionally, plants are able to undergo morphological changes and respond to environmental changes by changing their competitive abilities above and below ground. Because the allocation of aboveground and underground parts affects the rate of resource acquisition, they have become an important feature of plant growth and competitive ability [
30].
In the competition experiment, parasitism by C. australis increased the X. spinosum biomass and decreased the biomass of X. italicum. Moreover, X. spinosum and X. italicum had different resistances to C. australis: X. spinosum had a strong resistance and X. italicum had a relatively weak resistance. However, X. spinosum and X. italicum showed an increase in their root-to-shoot, stem, and leaf biomass ratios after the parasitism of C. australis, and their fruit biomass ratio decreased.
Two hypotheses are related to environmental change and plant biomass allocation: the growth−defense trade-off hypothesis and the resource availability hypothesis. The growth−defense trade-off hypothesis suggests that there is a trade-off between plant growth and defense, that is, when plants are stressed by biological factors, such as temperature, water, and nutrients, or harmed by biological factors, such as herbivores and insects in adverse environments, they will reduce their investment in their growth and increase their investment in defense capabilities, such as increasing defense materials [
31,
32]. The resource availability hypothesis suggests that the relationship between natural enemies and resource availability can lead to changes in plant growth−defense trade-offs [
33,
34,
35].
The changes in the biomass allocation of X. spinosum and X. italicum parasitized by C. australis demonstrated that X. spinosum and X. italicum reduced the biomass allocation of their fruits after being parasitized by C. australis and instead increased the biomass input of their roots, stems, and leaves. This is the result of invasive plants resisting natural enemies and environmental changes after entering new habitats. Therefore, the parasitic relationship between C. australis and X. spinosum, as well as X. italicum, supports the growth−defense trade-off and resource availability hypotheses. This investment trade-off benefits the survival, expansion, and rapid evolution of X. spinosum and X. italicum.
Competitive ability determines whether invasive plants successfully settle, reproduce, and spread after entering new habitats [
36,
37]. A strong competitive ability is conducive to resource competition between invasive plants, and a weak competitive ability is detrimental to invasive plants [
38]. Moreover, views on the impact of parasitic plants on the competitive ability of invasive plants, such as improving competitive ability, reducing competitive ability, or maintaining stability, differ [
39]. In the experiment on the impact of
C. australis parasitism on the competitive ability of
X. spinosum and
X. italicum, the RCI of
X. spinosum parasitized during the flowering and fruit stages was negative, and there was a significant difference from 0. Therefore, the parasitic relationship between
C. australis and
X. spinosum supports the evolutionary hypothesis of enhancing competitiveness. The parasitic relationship between
C. australis and
X. italicum during the seedling and flowering stages of
C. australis also supports the evolutionary hypothesis of reduced competitiveness because the RCI calculated based on the total biomass per plant was positive and significantly different from 0.
Parasitism by
C. australis affects the growth cycle of two invasive weeds of the genus Xanthium, to some extent, by absorbing nutrients and water. The results showed that
C. australis parasitism significantly shortened the growth cycle of the two invasive weeds and significantly advanced the flowering time, fruiting time, fruit ripening time, biomass, plant height, and crown width. Individual height is an important physiological and ecological characteristic of plants and is closely related to their life history [
40]. Plant height is an important trait that measures plant function and reflects the nutrient balance between plant growth and reproduction, affecting plant phenology [
41]. Studies have shown [
42] that increasing plant height delays its flowering phenology, and plants with shorter plant heights enter the reproductive period earlier to avoid competition with taller plants for light [
43,
44]. This is consistent with the following:
C. australis parasitism in this experiment resulted in a decrease in the plant height of the two invasive weeds and an earlier flowering time for the two invasive weeds.
5. Conclusions
Compared with the control, parasitism by C. australis increased the biomass of X. spinosum, and the biomass of X. italicum decreased. This indicates that X. spinosum has higher resistance to C. australis than X. italicum does. Under parasitism by C. australis, the root-to-shoot, stem, and leaf biomass ratios of X. spinosum and X. italicum increased, and the fruit biomass ratio decreased, indicating that C. australis parasitism changed the biomass distribution of X. spinosum and X. italicum. When C. australis parasitized during the flowering and fruit stages, the RCI of X. spinosum, calculated based on the total biomass of a single plant, was negative, indicating that C. australis parasitized to enhance the competitive ability of X. spinosum. When C. australis parasitized during the seedling and flowering stages, the RCI of Italian X. italicum calculated based on the total biomass per plant was positive, indicating that C. australis parasitized and reduced the competitiveness of Italian X. italicum. When experiencing the parasitism of C. australis, the growth cycle of X. spinosum and X. italicum was shortened, especially in the fruit stage. Additionally, the parasitism of C. australis significantly advanced the flowering time, fruiting time, and fruit ripening time of X. spinosum and X. italicum. The parasitism of C. australis significantly reduced the biomass, plant height, and crown width of X. spinosum and X. italicum. Thus, the parasitic effect of C. australis on the growth cycle of X. spinosum and X. italicum was mainly manifested by shortening and advancing the growth cycle of X. spinosum and X. italicum and reducing their biomass and other growth indicators.