Biol Invasions (2009) 11:835–844 DOI 10.1007/s10530-008-9297-z
ORIGINAL PAPER
Native Cuscuta campestris restrains exotic Mikania micrantha and enhances soil resources beneficial to natives in the invaded communities Hua Yu Æ Wei-Ming He Æ Jian Liu Æ Shi-Li Miao Æ Ming Dong
Received: 13 December 2007 / Accepted: 3 June 2008 / Published online: 20 June 2008 Ó Springer Science+Business Media B.V. 2008
Abstract Nutrients in exotic species and invaded communities play a key role in determining the dynamics of invaders and the invasibility of a receipt community. This study focused on the effects of the native holoparasite Cuscuta campestris (for short Cuscuta) on nutrients in the exotic invasive Mikania micrantha (for short Mikania) and stands invaded by Mikania. We conducted a set of field investigations on Mikania with Cuscuta parasitism for 1–4 years, and measured soil properties, community composition, and the growth and nutrient content of Mikania and Cuscuta in two types of sub-communities (i.e. with Mikania only, or with Mikania and Cuscuta). Cuscuta dramatically reduced the cover, biomass, and nutrients (i.e. N, P, and K content) of Mikania, significantly enhanced soil water, pH and nutrient content (i.e.
organic matter, total N and P, available P and K), and greatly increased the cover and species richness of native plants. In addition, N and K of Cuscuta were positively correlated with N of Mikania, which was negatively associated with soil total N, available P and K. These findings suggest that Cuscuta may be an effective measure against Mikania and be beneficial to the restoration of invaded communities. Keywords Biological control Community recovery Exotic invasive species Host-parasite interaction Nutrient process Plant-soil continuum
Introduction H. Yu W.-M. He (&) J. Liu S.-L. Miao M. Dong (&) State Key Laboratory of Vegetation and Environmental Change, Institute of Botany, Chinese Academy of Sciences, Beijing 100093, China e-mail:
[email protected] M. Dong e-mail:
[email protected] H. Yu Graduate University of Chinese Academy of Sciences, Beijing 100049, China J. Liu Institute of Environment Research, Shandong University, Ji’nan 250100, China
Biological invasions have posed threats to biodiversity and ecosystem function worldwide (Alpert et al. 2000; Davis et al. 2000; Ehrenfeld 2003; Callaway and Ridenour 2004). This has intensified studies on the control of exotic invaders (Elton 1958; Alpert 2006; Blumenthal 2006; Thomas and Reid 2007). The introduction of pathogens, parasites, and predators against invaders is expensive and risky, thereby limiting the feasibility of the introduction of natural enemies (Wright et al. 2005; Ding et al. 2006). Thus, efforts have focused on benign native solutions (Sheley and Krueger-Mangold 2003; Henderson et al. 2006; Richardson et al. 2007).
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Previous studies have shown that native parasites can limit exotic invaders escaping from their natural enemies and have fewer negative effects on nontarget species (Sheldon and Creed 1995; Torchin and Mitchell 2004; Krakau et al. 2006; Lian et al. 2006; Mitchell et al. 2006). Research has been dominated by laboratory studies. Lack of studies within natural communities has left many aspects of parasitic plants poorly studied (Pennings and Callaway 2002). Although native parasites can control invaders effectively, more efforts are necessary to understand the exact mechanisms by which parasites control exotic invaders. For example, soil nutrient availability is one of key factors in determining the invasion potential of exotic plants and the invasibility of local communities (Alpert et al. 2000; Ehrenfeld 2004; Howard et al. 2004; Hayes and Barry 2008). However, to our knowledge, little is known about the effects of native parasites on nutrient processes in invaded communities. Mikania micrantha (Compositae, hereafter referred to as Mikania) is among the 100 most notorious invaders in the world (Lowe et al. 2001). Since its first reported occurrence in the early 1980s, Mikania has invaded a broad range of habitats in southern China, resulting in tremendous economic and environmental losses (Li et al. 2000, 2006; Wang et al. 2004; Zhang et al. 2004). Increasing evidence has shown that the native holoparasite Cuscuta campestris (Convolvulaceae, hereafter referred to as Cuscuta) is an effective means to control Mikania (Wang et al. 2004; Shen et al. 2005, 2007), since it was first reported that Cuscuta parasitized and restrained Mikania in the fields of southern China in 2000 (Liao et al. 2002; Zan et al. 2002). Cuscuta decreased the photosynthesis and biomass production of Mikania (Shen et al. 2007), inhibited its flowering and reproduction (Deng et al. 2003; Shen et al. 2005), and changed its biomass allocation (Lian et al. 2006). Yet the effects of Cuscuta on nutrient patterns in Mikania and soil have not been examined explicitly. An understanding of nutrient changes in exotic species and invaded stands is important to detect the dynamics of invaders and to propose successful management strategies (Buckley et al. 2003). Parasitic plants restrain the growth and reproduction of their hosts by capturing nutrients and disturbing resource balance (Parker and Riches 1993; Benvenuti
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et al. 2005; Press and Phoenix 2005). The changes in resources impact the competition balance between native and invasive plants (Harris and Facelli 2003; Rickey and Anderson 2004), and increased nutrients facilitate the growth and competition of non-host species over parasitized hosts (Phoenix and Press 2005; Press and Phoenix 2005). Here, we hypothesize that the parasite Cuscuta might have dramatic effects on nutrient processes in Mikania and invaded soil, thereby suppressing the invasive Mikania, favoring the growth and competition of native plants, and contributing to the restoration of invaded plant communities. To test this hypothesis, a set of field investigations were conducted on the Neilingding Island in southern China. We chose two types of sub-communities with Mikania only, or with Mikania treated by Cuscuta for 1–4 years, and measured the composition and species richness of native plant communities, the growth and nutrient content of Mikania and Cuscuta, and soil properties. Our hypothesis predicts: (i) parasitism by Cuscuta inhibits the growth and nutrient content of Mikania, resulting in its decline and poor performance in nutrient competition, and (ii) this inhibition can enhance soil resource availability and increase the competition and survival of native plants, thereby, contributing to recovery of the invaded native plant community.
Methods Study site The field investigation was conducted on the Neilingding Island (113°470 –113°490 E, 22°240 – 0 22°26 N) in Guangdong Province, China. This area is characterized by oceanic monsoon, evergreen broadleaved forests, and sandy and gravelly soil. The basic traits of soil are presented in Table 1. Mikania was introduced to this island in 1984, since then, it has been extending rapidly, thereby invading orchards and forest margins (Li et al. 2000, 2006). Field investigation Each January from 2002 to 2005, about 10 kg mixture of live Cuscuta and parasitized Mikania tissues was collected from the Mikania-invaded community in
Native Cuscuta campestris restrains exotic Mikania micrantha Table 1 The initial soil traits (without Mikania and Cuscuta) of four sites on the Neilingding Island
Variable
837
Years since treated 1
pH
2
3
4
4.95 ± 0.19
4.88 ± 0.16
5.26 ± 0.12
5.59 ± 0.15
Water content (%)
23.76 ± 1.11
24.27 ± 0.78
21.50 ± 0.76
19.31 ± 1.10
Organic matter (g kg-1) Total N (g kg-1)
63.46 ± 2.26 5.30 ± 0.19
62.28 ± 2.29 3.87 ± 0.26
53.25 ± 1.52 3.94 ± 0.13
64.38 ± 1.75 4.03 ± 0.20
Total P (g kg-1)
1.07 ± 0.06
0.66 ± 0.06
0.73 ± 0.05
1.14 ± 0.08
Available P (mg kg-1)
6.24 ± 0.33
5.05 ± 0.32
6.37 ± 0.21
Available K (mg kg-1)
456.1 ± 12.9
456.2 ± 9.6
7.72 ± 0.25
295.4 ± 14.9
284.6 ± 9.8
C:N ratio
8.17 ± 0.27
10.99 ± 0.47
9.22 ± 0.45
10.91 ± 0.19
N:P ratio
10.62 ± 0.53
12.61 ± 1.16
11.57 ± 0.26
7.63 ± 0.21
Shenzhen, and released to a 3.0 9 3.0 m2 plot in the centre of a selected Mikania-invaded community on the Neilingding Island. The four receipt communities were several 100 m away from each other. Once introduced, Cuscuta grew vigorously and spread at the speed of 35-200% per year (Wang et al. 2004). After killing a Mikania plant, Cuscuta would infect others. By January 2006, the introduction created four stages of communities parasitized by Cuscuta for 1–4 years. After four years of parasitism, 80% of Mikania in treated communities was parasitized by Cuscuta. Based on the regimes of Mikania and Cuscuta, each Cuscuta-parasitized community was divided into two sub-communities, that is, the central sub-community with Mikania and Cuscuta simultaneously (also referred to as Cuscuta-treated) and outer sub-community with Mikania only (also referred to as Mikania-invaded). In mid-January 2006, we set up three 1.0 9 1.0 m2 quadrats in each sub-community to determine species number and percent cover of vascular plants. For both Mikania-invaded and Cuscuta-treated sub-communities, five Mikania individuals were randomly selected and their aboveground parts were harvested; Cuscuta was separated from Mikania. All plant materials were dried at 80°C for 48 h, weighed, and ground into a fine powder for the measurement of nitrogen (N), phosphorus (P), and potassium (K). To examine the effects of Cuscuta parasitism on soil traits, soil samples were collected within three 1.0 9 1.0 m2 quadrats per sub-community, from the depths of 0 to 10 cm. Each quadrat had five sampling points, and soil samples from each quadrat were composited and treated as a single sample (Falkengren-Grerup et al. 2006), before determining its pH, water content, organic matter, total N, total and
available P, and available K. There were three replicates for soil samples. Sample analyses Each soil sample was divided into three portions. One portion was stored in containers for the measurement of soil water content, and the other two portions were air-dried at room temperature, ground, and sieved with a 2- or 0.8-mm sieve for the measurements of pH and nutrients. Soil water was determined by drying at 105°C for 48 h. pH was measured through extracting 10 g soil with 25 ml 0.2 mol/l KCl. Organic matter was determined using dichromate oxidation (Nelson and Sommers 1982). Extracts of soil samples digested in sulphuric acid–hydrogen peroxide with Se as a catalyst, were used for the analyses of total N and P. Total N was determined with the Kjeldahl distillation method (Bremner and Mulvaney 1982). Total P was determined using the colorimetric molybdenum blue method with a Hitachi U-2000 spectrophotometer (Olsen and Sommers 1982). Available P was determined using the Bray1 method (0.03 mol/l NH4F + 0.025 mol/l HC1) (Bray and Kurtz 1945; Holford 1997), and available K was analyzed with atomic absorption spectrophotometry (Michelsen et al. 1999). The ratios of C:N and N:P were expressed as atomic ratios. The samples of Cuscuta and Mikania were dried at 80°C for 48 h, ground, and sieved with a 2-mm sieve. About 0.1 g plant materials were digested in 5 ml 98% H2SO4 with 20 mg H3SeO4 and 1 ml 30% H2O2 for the analyses of N, P, and K. N was analyzed colorimetrically with the Kjeldahl acid-digestion method using an Alpkem auto-analyzer (Kjektec
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System 1026 distilling unit, Sweden), P was analyzed with the molybdenum blue method using a Hitachi U2000 spectrophotometer (Allen 1989), and K was analyzed with atomic absorption spectrophotometry using a Perkin Elmer AAS 4100 (Michelsen et al. 1999). Data analyses The growth and nutrient content of Mikania, the cover of native species, the species richness of native communities, and soil properties were analyzed using two-way ANOVA followed by Turkey’s HSD test, with treatment (with or without Cuscuta) and time since Cuscuta application as fixed factors. The growth and nutrient content of Cuscuta were analyzed with one-way ANOVA. Spearman correlation coefficients were calculated to determine correlations of the nutrient changes in Cuscuta, Mikania, and soil. All the statistical analyses were conducted with SPSS 13.0 software.
Results Cuscuta dramatically reduced the cover, biomass, N, P, and K content of Mikania (Fig. 1; all P \ 0.05), but had a slight effect on N:P ratio (Fig. 1f; P [ 0.05). Although these six traits of Mikania significantly varied with time since Cuscuta application (all P \ 0.05), there were differences in changing patterns. Except for P, there existed significant interactions between Cuscuta effects and treatment time for the other five traits (Fig. 1). Cuscuta significantly enhanced soil traits (all P \ 0.05), except for C:N ratio (Fig. 2). For all these soil traits, there were significant interactions between Cuscuta effects and time since its introduction (Fig. 2; all P \ 0.05). Different soil traits exhibited contrasting responses to Cuscuta effects. For example, pH, organic matter, total N and P, available K, C:N ratio, and N:P ratio did not respond after one year of parasitism, but the opposite was the case for other traits, with an increase in available P and a decrease in water content (Fig. 2). Cuscuta greatly enhanced the cover of native plants and species richness of native communities (Fig. 3; all P \ 0.05), and its effects increased with time since parasitism (all P \ 0.05). The cover,
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biomass, N and K content, and N:P ratio of Cuscuta significantly varied with time (Fig. 4; all P \ 0.05), with an exception for P (Fig. 4d; P = 0.722). The cover and biomass peaked after two years of parasitism (Fig. 4a, b), N and K content peaked after three years of parasitism (Fig. 4c, e), and N:P peaked after four years of parasitism (Fig. 4f). N and N:P ratio showed similar patterns over time. Soil total N was negatively correlated with N of Mikania and Cuscuta; soil available P was negatively correlated with N of Mikania; soil available K was negatively correlated with N of Mikania and Cuscuta, P of Mikania, and K of Cuscuta (Table 2). N of Cuscuta was positively correlated with N of Mikania, and negatively with P of Mikania; K of Cuscuta was positively correlated with N of Mikania (Table 2).
Discussion Our findings support the hypothesis that the native holoparasite Cuscuta confers dramatic effects on nutrient processes in Mikania and soil. Cuscuta suppressed the growth and nutrients of Mikania, enhanced soil resources, and positively impacted native communities. Additionally, such effects of Cuscuta tended to increase over time. These changes had dramatic impacts on the growth of Cuscuta. Thus, Cuscuta might alter nutrient cycling in the invaded communities through changing nutrient allocation within plant-soil continuum. Previous studies have shown that parasitic plants play an important role in community organization and function (Pennings and Callaway 1996, 2002; Callaway and Pennings 1998; Press and Phoenix 2005; March and Watson 2007). Although there were complex correlations between nutrients within Mikania, Cuscuta and soil, there were some clear patterns. For example, N and K of Cuscuta were positively correlated with N of Mikania, which was negatively correlated with soil N, P, and K. These correlations imply that soil nutrient availability may not be a promoter for the invasion of Mikania with the presence of Cuscuta, but the succession of Cuscuta is dependent on the N availability of its host Mikania, since parasitic plants capture solute flux from their hosts (Hibberd and Jeschke 2001). Actually, the growth of Cuscuta declined with time due to the decrease in Mikania
Native Cuscuta campestris restrains exotic Mikania micrantha
839
(a)
(b)
(c)
(d)
(e)
(f)
Fig. 1 Percent cover per quadrat (a), biomass per individual (b), N content (c), P content (d), K content (e), and N:P ratio (f) of Mikania untreated (open) or treated (hatched) by Cuscuta for 1–4 years. Data are means ± SE (n = 3). F-values and
significance levels (*** P \ 0.001, ** P \ 0.01, * P \ 0.05, and ns P C 0.05) are given. T = Cuscuta treatment, and t = time since Cuscuta application
growth. Interestingly, Cuscuta P remained unchanged over time, thus N:P ratios highly depended on the change in its N. Cuscuta greatly reduced the growth and nutrients of its host Mikania. These findings agree with the results by Jeschke and Hilpert (1997), but disagree with those by Alcantara et al. (2006). Rapid growth and high nutrient contents are the traits associated with invasiveness of exotic invaders (Alpert et al. 2000; Liu et al. 2006; Herron et al. 2007), and invasive plants tend to outperform coexisting native species in nutrient competition (Daehler 2003; Zedler and Kercher 2004; Funk and Vitousek 2007). However, parasitic plants greatly depend on nutrients of their hosts and their parasitism often severely suppresses host performance, changing the competition balance and facilitating the
non-host species over their hosts (Phoenix and Press 2005; Press and Phoenix 2005). Thus, the restraints to growth and nutrients of Mikania by Cuscuta imply its declined invasiveness and decreased competitive ability over native plants. The above-ground effects driven by parasitic plants often have important indirect consequences on soil resources (Bardgett et al. 2006). Interestingly, Cuscuta conferred limited impacts on soil nutrients following 1year infection in this study. For example, soil nutrients had no response to Cuscuta parasitism with an exception of soil available P. The reasons may be linked to the growth regime of Cuscuta and the capability of Mikania to take up soil nutrients. Specifically, Cuscuta grew relatively slowly at the early stage of infection (i.e. low abundance), conferring low inhibitory effects on the
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H. Yu et al.
(a)
(b)
(c)
(d)
(e)
(f)
(g)
(h)
(I)
Fig. 2 Soil properties (i.e. pH, water content, organic matter, total N, total P, available P, available K, C:N ratio, and N:P ratio) in communities Mikania-invaded (open) or Cuscutatreated (hatched) for 1–4 years. Data are means ± SE (n = 3).
(a)
F-values and significant levels (*** P \ 0.001, ** P \ 0.01, * P \ 0.05, and ns P C 0.05) are given. T = Cuscuta treatment, and t = time since Cuscuta application
(b)
Fig. 3 Percent cover of native plants (a) and species richness of native communities (b) with Mikania-invaded (open) or Cuscuta-treated (hatched) for 1–4 years. Data are means ± SE
(n = 3). F-values and significance levels (*** P \ 0.001, ** P \ 0.01, * P \ 0.05, and ns P C 0.05) are given. T = Cuscuta treatment, and t = time since Cuscuta application
growth of Mikania. However, as indicated by Mikania growth and soil traits, the effects of Cuscuta intensified over time, significantly impacting soil nutrients after 2year parasitism.
Overall, Cuscuta dramatically increased soil nutrients, which was linked to its effective suppression on Mikania. Litters of invaders have higher nutrient concentration and more efficient decomposition than
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Native Cuscuta campestris restrains exotic Mikania micrantha
841
(a)
(b)
(c)
(d)
(e)
(f)
Fig. 4 Percent cover (a), biomass (b), N content (c), P content (d), K content (e), and N:P ratio (f) of Cuscuta parasitizing Mikania for 1–4 years on the Neilingding Island. Data are
means ± SE (n = 3). Bars sharing the same letters are not statistically significant at P = 0.05
Table 2 Correlations between nutrients (N, P, and K content) in Mikania, Cuscuta, and soil Variable Soil N Soil P Soil K
Soil N
Soil P
0.759** -0.630*
Mik P Mik K Cus P Cus K
Mik N
Mik P
Mik K
Cus N
Cus P
Cus K
1 -0.446ns
Mik N
Cus N
Soil K
1 -0.026ns
1
-0.617*
-0.644*
0.451ns
-0.060
-0.671*
-0.544ns
0.358ns
-0.427ns
0.532ns
0.148ns
0.470ns
-0.942**
0.686*
-0.691*
-0.475ns
ns
ns
ns
-0.671** ns
0.347
-0.497
ns
ns
0.086
ns
-0.343
ns
-0.410
0.340
ns
-0.835**
1
-0.065
0.892**
1
0.256
ns
-0.527
1 0.198
ns
0.074
1 -0.213ns 0.862**
1 -0.151ns
1
Notes: Mik, Mikania; Cus, Cuscuta * P \ 0.05, ** P \ 0.01, and
ns
P C 0.05
co-occurring natives (Ehrenfeld 2003). Parasitic plants are able to enhance the decomposition of litters, and transform nutrients from more recalcitrant or less available forms to those more labile and available (Phoenix and Press 2005; Press and Phoenix 2005). Additionally, a severely affected host has a limited capacity to assimilate soil nutrients (Phoenix and Press 2005). Mikania suppressed by Cuscuta indicates its limited nutrient capture. Thus, the impact of Cuscuta on Mikania increased soil resource availability, facilitating the natives over the invader. It supports the notion that parasitic plants impact soil resources available to non-host plants (Press and
Phoenix 2005; Bardgett et al. 2006), and that control of invasive species results in increased resources available for native species (Harris and Facelli 2003). Nutrient changes have key effects on the composition of plant communities and determine their invasibility (Gough et al. 2000; De Deyn et al. 2004). Increased resources contribute to species richness and facilitate the coexistence of multiple species (Tilman et al. 1997; Press and Phoenix 2005). Cuscuta significantly increased the growth and species richness of native plants in this study. This is linked to two aspects: Mikania, suppressed by Cuscuta, has diminished competitive ability, or
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limited demand for soil resources. On the other hand, increased soil resource availability, due to Cuscuta parasitism, is favorable for the competition and survival of the non-host native species. Previous studies have shown that enhanced soil nutrients facilitate the growth and competition of native plants over the stressed invaders (Harris and Facelli 2003; Rickey and Anderson 2004). When Cuscuta was absent, Mikania exhibited profound effects on the soil system and created favorable conditions for its invasion (Li et al. 2006). However, when Cuscuta was introduced to Mikania-invaded communities, the vigorous parasitism of Cuscuta was suppressive or even fatal to Mikania (Wang et al. 2004; Shen et al. 2005, 2007). Once target invasive plants were suppressed, native species with invasionresistance would utilize soil resources to amplify their fitness and resistance, and even to suppress the re-growth of invaders (Weis and Hochberg 2000). The control of invaders facilitates the restoration of introduced communities (Tilman et al. 1997; Herben et al. 2004). In this study, the application of Cuscuta had positive effects on native plant communities, as indicated by cover and species richness of native plants. In nature, native plants were obviously enhanced in the invaded communities and Mikania followed the opposite direction due to the introduction of Cuscuta (Liao et al. 2002; Zan et al. 2002; Wang et al. 2004). Previous studies have exhibited that Cuscuta mainly infects the invasive plant Mikania and has no significant side effect on native species, although it parasitizes some natives at low infection rates after Mikania is restrained (Zan et al. 2003). As a minor component of local plant communities, Cuscuta exerts no threat to native plants or catastrophic consequence on native communities (Wang et al. 2004). In conclusion, these findings show that the native parasite Cuscuta has dramatic effects on nutrient processes by changing nutrient regimes in Mikania and soil in the invaded communities. These changes inhibit the growth and invasiveness of Mikania, and facilitate the survival and competition of non-host native species over the invasive host. Consequently, Cuscuta may be an effective measure to control Mikania and to restore invaded plant communities. It is most likely that the host-parasite interactions between exotic invaders and native parasites provide an effective and environmentally benign measure to combat against exotic invasions.
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H. Yu et al. Acknowledgements We are grateful to Feihai Yu and Shumin Zhang for their help on experimental design, Susan M. Carstenn, Chris Edelstein and Sara Neugaard for polishing this manuscript, Qijie Zan and Aiping Wu for their assistance during field investigation. This study was supported by the program entitled Oversea Distinguished Scholars of the Chinese Academy of Sciences (58246G1215) and by the Grant from the National Natural Science Foundation of China (30770335).
References Alcantara E, Morales-Garcia M, Diaz-Sanchez J (2006) Effects of broomrape parasitism on sunflower plants: growth, development, and mineral nutrition. J Plant Nutr 29:1199– 1206. doi:10.1080/01904160600767351 Allen SE (1989) Chemical analysis of ecological materials. Blackwell Scientific Publications, Oxford Alpert P (2006) The advantages and disadvantages of being introduced. Biol Invasions 8:1523–1534. doi:10.1007/s10530005-5844-z Alpert P, Bone E, Holzapfel C (2000) Invasiveness, invasibility, and the role of environmental stress in preventing the spread of non-native plants. Perspect Plant Ecol Evol Syst 3:52–66. doi:10.1078/1433-8319-00004 Bardgett RD, Smith RS, Shiel RS, Peacock S, Simkin JM, Quirk H et al (2006) Parasitic plants indirectly regulate below-ground properties in grassland ecosystems. Nature 439:969–972. doi:10.1038/nature04197 Benvenuti S, Dinelli G, Bonetti A, Catizone P (2005) Germination ecology, emergence and host detection in Cuscuta campestris. Weed Res 45:270–278. doi:10.1111/j.13653180.2005.00460.x Blumenthal DM (2006) Interactions between resource availability and enemy release in plant invasion. Ecol Lett 9:887–895. doi:10.1111/j.1461-0248.2006.00934.x Bray RH, Kurtz LT (1945) Determination of total, organic, and available forms of phosphorus in soils. Soil Sci 59:39–45. doi:10.1097/00010694-194501000-00006 Bremner JM, Mulvaney CS (1982) Nitrogen-total. In: Page AL, Miller RH, Keeney DR (eds) Methods of soil analysis (part 2), 2nd edn. ASA, Madison, pp 595–624 Buckley YM, Downey P, Fowler SV, Hill R, Memmot J, Norambuena H et al (2003) Are invasives bigger? A global study of seed size variation in two invasive shrubs. Ecology 84:1434–1440. doi:10.1890/0012-9658(2003)084[1434:AI BAGS]2.0.CO;2 Callaway RM, Pennings SC (1998) Impact of a parasitic plant on the zonation of two salt marsh perennials. Oecologia 114:100–105. doi:10.1007/s004420050425 Callaway RM, Ridenour WM (2004) Novel weapons: invasive success and the evolution of increased competitive ability. Front Ecol Environ 2:436–443 Daehler CC (2003) Performance comparisons of co-occurring native and alien invasive plants: implications for conservation and restoration. Annu Rev Ecol Evol Syst 34:183– 211. doi:10.1146/annurev.ecolsys.34.011802.132403 Davis MA, Grime JP, Thompson K (2000) Fluctuating resources in plant communities: a general theory of
Native Cuscuta campestris restrains exotic Mikania micrantha
843
invasibility. J Ecol 88:528–534. doi: 10.1046/j.1365-2745.2000.00473.x De Deyn GB, Raaijmakers CE, Van der Putten WH (2004) Plant community development is affected by nutrients and soil biota. J Ecol 92:824–834. doi:10.1111/j.0022-0477. 2004.00924.x Deng X, Feng HL, Ye WH, Yang QH, Xu KY, Cao HL et al (2003) A study on the control of exotic weed Mikania micrantha by using parasitic Cuscuta campestris. J Trop Subtrop Bot 11:117–122 Ding JQ, Reardon R, Wu Y, Zheng H, Fu WD (2006) Biological control of invasive plants through collaboration between China and the United States of America: a perspective. Biol Invasions 8:1439–1450. doi:10.1007/s 10530-005-5833-2 Ehrenfeld JG (2003) Effects of exotic plant invasions on soil nutrient cycling processes. Ecosystems (N Y, Print) 6:503–523. doi:10.1007/s10021-002-0151-3 Ehrenfeld JG (2004) Implications of invasive species for belowground community and nutrient. Weed Technol 18:1232–1235 Elton C (1958) The ecology of invasions by animals and plants. Methuen, London Falkengren-Grerup U, Brink DJ, Brunet J (2006) Land use effects on soil N, P, C and pH persist over 40–80 years of forest growth on agricultural soils. For Ecol Manage 225:74–81. doi:10.1016/j.foreco.2005.12.027 Funk JL, Vitousek PM (2007) Resource-use efficiency and plant invasion in low-resource systems. Nature 446:1079– 1081. doi:10.1038/nature05719 Gough L, Osenberg CW, Gross KL, Collins SL (2000) Fertilization effects on species density and primary productivity in herbaceous plant communities. Oikos 89:428–439. doi: 10.1034/j.1600-0706.2000.890302.x Harris MR, Facelli JM (2003) Competition and resource availability in an annual plant community dominated by an invasive species, Carrichtera annua (L. Aschers.), in South Australia. Plant Ecol 167:19–29. doi:10.1023/A: 1023981500007 Hayes KR, Barry SC (2008) Are there any consistent predictors of invasion success? Biol Invasions 10:483–506. doi: 10.1007/s10530-007-9146-5 Henderson S, Dawson TP, Whittaker RJ (2006) Progress in invasive plants research. Prog Phys Geogr 30:25–46. doi: 10.1191/0309133306pp468ra Herben T, Mandak B, Bimova K, Munzbergova Z (2004) Invasibility and species richness of a community: a neutral model and a survey of published data. Ecology 85:3223– 3233. doi:10.1890/03-0648 Herron PM, Martine CT, Latimer AM, Leicht-Young SA (2007) Invasive plants and their ecological strategies: prediction and explanation of woody plant invasion in New England. Divers Distrib 13:633–644 Hibberd JM, Jeschke WD (2001) Solute flux into parasitic plants. J Exp Bot 52:2043–2049. doi:10.1093/jexbot/ 52.363.2043 Holford ICR (1997) Soil phosphorus: its measurement, and its uptake by plants. Aust J Soil Res 35:227–239. doi: 10.1071/S96047 Howard TG, Gurevitch J, Hyatt L, Carreiro M, Lerdau M (2004) Forest invasibility in communities in southeastern
New York. Biol Invasions 6:393–410. doi: 10.1023/B:BINV.0000041559.67560.7e Jeschke WD, Hilpert A (1997) Sink-stimulated photosynthesis and sink-dependent increase in nitrate uptake: nitrogen and carbon relations of the parasitic association Cuscuta reflexa-Ricinus communis. Plant Cell Environ 20:47–56. doi:10.1046/j.1365-3040.1997.d01-2.x Krakau M, Thieltges DW, Reise K (2006) Native parasites adopt introduced bivalves of the North Sea. Biol Invasions 8:919–925. doi:10.1007/s10530-005-4734-8 Li MG, Zhang WY, Liao WB, Wang BS, Zan QJ (2000) The history and status of the study on Mikania micrantha. Ecol Sci 19:41–45 Li WH, Zhang CB, Jiang HB, Xin GR, Yang ZY (2006) Changes in soil microbial community associated with invasion of the exotic weed, Mikania micrantha H.B.K. Plant Soil 281:309–324. doi:10.1007/s11104-005-9641-3 Lian JY, Ye WH, Cao HL, Lai ZM, Wang ZM, Cai CX (2006) Influence of obligate parasite Cuscuta campestris on the community of its host Mikania micrantha. Weed Res 46:441–443. doi:10.1111/j.1365-3180.2006.00538.x Liao WB, Fan Q, Wang BX, Wang YJ, Zhou XY (2002) Discovery of three species of Cuscuta harming Mikania micrantha in South China and their taxonomical identification. Acta Sci Nat Univ Sunyatseni 41:54–56 Liu J, Dong M, Miao SL, Li ZY, Song MH, Wang RQ (2006) Invasive alien plants in China: role of clonality and geographical origin. Biol Invasions 8:1461–1470. doi: 10.1007/s10530-005-5838-x Lowe S, Browne M, Boudjelas S, Poorter MD (2001) 100 of the world’s worst invasive alien species. A selection from the global invasive species database. IUCN/SSC Invasive Species Specialist Group (ISSG), Auckland, New Zealand March WA, Watson DM (2007) Parasites boost productivity: effects of mistletoe on litterfall dynamics in a temperate Australian forest. Oecologia 154:339–347. doi:10.1007/ s00442-007-0835-7 Michelsen A, Graglia E, Schmidt IK, Jonasson S, Sleep D, Quarmby C (1999) Differential responses of grass and a dwarf shrub to long-term changes in soil microbial biomass C, N and P following factorial addition of NPK fertilizer, fungicide and labile carbon to a heath. New Phytol 143:523–538. doi:10.1046/j.1469-8137.1999. 00479.x Mitchell CE, Agrawal AA, Bever JD, Gilbert GS, Hufbauer RA, Klironomos JN et al (2006) Biotic interactions and plant invasions. Ecol Lett 9:726–740. doi:10.1111/ j.1461-0248.2006.00908.x Nelson DW, Sommers LE (1982) Total carbon, organic carbon, and organic matter. In: Page AL, Miller RH, Keeney DR (eds) Methods of soil analysis (part 2), 2nd edn. ASA, Madison, pp 539–580 Olsen SR, Sommers LE (1982) Phosphorus. In: Page AL, Miller RH, Keeney DR, Page AL, Miller RH, Keeney DR (eds) Methods of soil analysis (part 2), 2nd edn. ASA, Madison, pp 403–430 Parker C, Riches CR (1993) Parasitic weeds of the world: biology and control. CAB Int., Wallingford Pennings SC, Callaway RM (1996) Impact of a parasitic plant on the structure and dynamics of salt marsh vegetation. Ecology 77:1410–1419. doi:10.2307/2265538
123
844 Pennings SC, Callaway RM (2002) Parasitic plants: parallels and contrasts with herbivores. Oecologia 131:479–489. doi:10.1007/s00442-002-0923-7 Phoenix GK, Press MC (2005) Linking physiological traits to impacts on community structure and function: the role of root hemiparasitic Orobanchaceae (ex-Scrophulariaceae). J Ecol 93:67–78. doi:10.1111/j.1365-2745.2004.00950.x Press MC, Phoenix GK (2005) Impacts of parasitic plants on natural communities. New Phytol 166:737–751. doi: 10.1111/j.1469-8137.2005.01358.x Richardson DM, Holmes PM, Esler KJ, Galatowitsch SM, Stromberg JC, Kirkman SP et al (2007) Riparian vegetation: degradation, alien plant invasions, and restoration prospects. Divers Distrib 13:126–139 Rickey MA, Anderson RC (2004) Effects of nitrogen addition on the invasive grass Phragmites australis and a native competitor Spartina pectinata. J Appl Ecol 41:888–896. doi:10.1111/j.0021-8901.2004.00948.x Sheldon SP, Creed RP (1995) Use of a native insect as a biological control for an introduced weed. Ecol Appl 5:1122–1132. doi:10.2307/2269359 Sheley RL, Krueger-Mangold J (2003) Principles for restoring invasive plant-infested rangeland. Weed Sci 51:260–265. doi:10.1614/0043-1745(2003)051[0260:PFRIPI]2.0.CO;2 Shen H, Ye WH, Hong L, Cao HL, Wang ZM (2005) Influence of the obligate parasite Cuscuta campestris on growth and biomass allocation of its host Mikania micrantha. J Exp Bot 56:1277–1284. doi:10.1093/jxb/eri128 Shen H, Hong L, Ye WH, Cao HL, Wang ZM (2007) The influence of the holoparasitic plant Cuscuta campestris on the growth and photosynthesis of its host Mikania micrantha. J Exp Bot 58:2929–2937. doi:10.1093/jxb/ erm168 Thomas MB, Reid AM (2007) Are exotic natural enemies an effective way of controlling invasive plants? Trends Ecol Evol 22:447–453. doi:10.1016/j.tree.2007.03.003
123
H. Yu et al. Tilman D, Knops J, Wedin D, Reich P, Ritchie M, Siemann E (1997) The influence of functional diversity and composition on ecosystem processes. Science 277:1300–1302. doi:10.1126/science.277.5330.1300 Torchin ME, Mitchell CE (2004) Parasites, pathogens, and invasions by plants and animals. Front Ecol Environ 2:183–190 Wang BS, Wang YJ, Liao WB, Zan QJ, Li MG, Peng SL, Han AC, Zhang WY, Chen DP (2004) The invasion ecology and management of alien weed Mikania micrantha H.B.K. Science Press, Beijing Weis AE, Hochberg ME (2000) The diverse effects of intraspecific competition on the selective advantage to resistance: a model and its predictions. Am Nat 156:276– 292. doi:10.1086/303386 Wright MG, Hoffmann MP, Kuhar TP, Gardner J, Pitcher SA (2005) Evaluating risks of biological control introductions: a probabilistic risk-assessment approach. Biol Control 35:338–347. doi:10.1016/j.biocontrol.2005.02.002 Zan QJ, Wang BS, Wang YJ, Liao WB, Li MG, Xu HL (2002) The ecological evaluation on the controlling Mikania micrantha by Cuscuta campestris. Acta Sci Nat Univ Sunyatseni 41:60–63 Zan QJ, Wang BS, Wang YJ, Zhang JL, Liao WB, Li MG (2003) The harm caused by Mikania micrantha and its control by Cuscuta campestris. J Plant Ecol 27:822–828 Zedler JB, Kercher S (2004) Causes and consequences of invasive plants in wetlands: Opportunities, opportunists, and outcomes. Crit Rev Plant Sci 23:431–452. doi: 10.1080/07352680490514673 Zhang LY, Ye WH, Cao HL, Feng HL (2004) Mikania micrantha H.B.K. in China—an overview. Weed Res 44:42–49
