JXB Advance Access originally published online on March 14, 2005
Journal of Experimental Botany 2005 56(415):1277-1284; doi:10.1093/jxb/eri128
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RESEARCH PAPER |
Influence of the obligate parasite Cuscuta campestris on growth and biomass allocation of its host Mikania micrantha
South China Botanical Garden, Chinese Academy of Sciences, Guangzhou 510650, PR China
* To whom correspondence should be addressed. Fax: +86 20 3725 2831. E-mail: why{at}scbg.ac.cn
Received 6 January 2005; Accepted 26 January 2005
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Abstract |
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As a means of biologically controlling Mikania micrantha H.B.K. in South China, the influence of the obligate parasite Cuscuta campestris Yuncker on its growth and biomass allocation was studied using pot trials. The effect of C. campestris on M. micrantha became greater with time, such that the host biomass was only 1.8% of the control after 60 d of parasitism and by day 72 almost all the aerial parts of the host plants had died. Afterwards, the hosts and the remnant parasite shoots re-grew but the total biomass of the hosts was still significantly lower than that of the controls. The infection by C. campestris greatly increased the shoot:root dry weight ratio and the allocation to stems of the infected plants from 40 to 50 d after parasitization, but decreased their relative growth rate and unit leaf rate starting from 20 d after parasitization and their leaf area ratio from 30 to 60 d after parasitization. Cuscuta campestris significantly reduced the total biomass, changed the biomass allocation patterns, and completely inhibited the flowering of the infected M. micrantha plants. These results indicate that the use of C. campestris could be a potentially effective way of controlling M. micrantha.
Key words: Biological control, Cuscuta campestris, growth, invasive species, Mikania micrantha, obligate parasite, parasitism
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Introduction |
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Biological invasion has been widely recognized and has received intense studies over the past half century (Elton, 1958
; Mooney and Drake, 1986; Vitousek et al., 1996; Mack et al., 2000; Kennedy et al., 2002). It has contributed to the worldwide loss of biodiversity in aquatic and terrestrial systems (Baker and Stebbins, 1965; Heywood, 1989), and it is an important element in global change (Lövei, 1997; Vitousek et al., 1997; Dukes and Mooney, 1999).
Mikania micrantha H.B.K. is a fast-growing perennial creeping vine belonging to the family Asteraceae and is native to Central and South America, where it is a weed of minor importance (Wirjahar, 1976; Holm et al., 1977). However, in its palaeotropic exotic range, it has become a major invader and notorious weed of agricultural land (Parker, 1972; Holm et al., 1977; Waterhouse, 1994; Cronk and Fuller, 1995; Zhang et al., 2004). It has been listed as one of the 100 worst invasive alien species in the world (Lowe et al., 2001), and it is considered the second most serious weed in the South Pacific (Waterhouse and Norris, 1987).
To reduce the damage caused by M. micrantha to tree crops or forest plantations, various management methods have been used, including cultural, mechanical, chemical, and biological controls (Parker, 1972; Cock et al., 2000; Ellison, 2001; Ellison et al., 2004; Zhang et al., 2004). Biological control is particularly attractive in controlling weeds in crops because biological agents applied do not adversely affect the non-target species as do chemical herbicides (CAB International Institute of Biological Control, 1987). It has been widely recognized as one of the most promising methods of controlling exotic species, especially when native species are used to control exotic invasive weeds.
Some studies have examined the effects of the obligate parasite Cuscuta campestris on M. micrantha in biomass production, physiology, and ecology (Deng et al., 2003; Zan et al., 2003; Chiu and Shen, 2004). Others have shown that Cuscuta spp., including C. campestris Yuncker, C. chinensis Lam., and C. australis R. Br., can effectively restrain the growth of M. micrantha, while C. campestris could cause the aerial parts to die (Parker, 1972; Liao et al., 2002; Zan et al., 2003; Chiu and Shen, 2004; Zhang et al., 2004). These studies have found that C. campestris prefers M. micrantha as a host. Moreover, although M. micrantha plants infected by C. campestris could flower, flowering was delayed and was less than on the uninfected plants. Thus, the use of C. campestris is potentially an effective way of controlling M. micrantha. However, it is not understood how C. campestris influences biomass accumulation and allocation, and the development of M. micrantha.
The genus Cuscuta (Convolvulaceae) is an obligate stem parasite (Parker and Riches, 1993; Dawson et al., 1994; Press, 1995b; Hibberd et al., 1998b). Cuscuta campestris is the most widespread species in the genus in the world and the only parasitic weed of North America that has spread to the Old World (Dawson et al., 1994). It obtains its resources entirely from its host plants, severely suppressing them and even resulting in their death (Ashton and Santana, 1976; Cooke and Black, 1987; Dawson et al., 1994). This parasite has a wide range of host species (Yuncker, 1932; Parker et al., 1984; Nemli, 1989). It mainly parasitizes alfalfa, but also attacks some horticultural crops, legumes, and broadleaved weeds, though it is seldom found on woody plants, grasses, or cereals (Dawson et al., 1994). In South China, it is distributed in Guangdong Province (Liao et al., 2002). Although it normally grows as an annual (Dawson et al., 1994), its shoots can stay alive in winter, and its seeds may germinate and then infect host plants in the following spring (Wang et al., 2002).
Mikania micrantha entered South China after 1910, and since the 1980s it has started to spread and invade widely (Zhang et al., 2004). It has caused severe damage to many ecosystems in Guangdong Province in recent years. Alarmed by the rapid spread and serious damage of M. micrantha, Chinese scientists are now looking for effective biological control options to deal with this deleterious plant. For such a purpose, this project was conducted to investigate the potential use of C. campestris to control M. micrantha and to study how C. campestris influences its growth and physiology in the field in South China.
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Materials and methods |
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Study site
The experiment was conducted during the June–December 2003 growing season at the field station (23°8' N, 113°17' E, 8 m asl) in Guangzhou, Guangdong Province, the People's Republic of China. The climate is lower subtropical.
Experimental materials and design
On 30 June 2003, whole M. micrantha plants were collected from a M. micrantha population in the suburb of Dongguan, Guangdong Province. Two-node segments, similar in size, were selected from the middle of the stems to minimize the influence of phenotypic maternal effects. The segments were planted in pots (50 cm in height, 50 cm in upper diameter and 45 cm in lower diameter) filled with a mixture of pool mud and paddy field clay (1:2 in volume). In each pot, three segments were planted with the lower node buried below and the upper one about 5 cm above the soil surface. The upper nodes began to sprout 3 d later. When the plants were about 170 cm tall on 23 August, they were thinned to one per pot and 240 individuals, similar in height and stem diameter, were selected as replicates and arranged in a completely randomized design. Half of them were randomly chosen to be inoculated with C. campestris (infected group), leaving the rest uninfected (control group). To prevent M. micrantha from climbing from one pot to another, pots were separated at least 1 m from each other and a bamboo cane about 4 m long was placed vertically in each pot for M. micrantha to climb on.
Seeds of C. campestris were collected from a single M. micrantha population on 10 January 2003 and stored at room temperature. On 12 August, the seeds were sown in pots with sand at a depth of c. 1 cm. Three days later, the seeds began to germinate and completed germination on 19 August. On 26 August, when M. micrantha plants were c. 180 cm tall and C. campestris seedlings were c. 5 cm tall, one C. campestris seedling was placed, together with wet sand, on the soil surface of each M. micrantha pot in the infected group. By 29 August, all the M. micrantha plants in this inoculated group had become infected with C. campestris stems. The experiment ended in December, 120 d after parasitization (DAP) or 180 d after planting, when the uninfected M. micrantha plants had started to wither. During the experiment, the pots were weeded when necessary and watered twice daily with tap water at 06.00 h and 18.00 h, except on rainy days.
Measurements of growth
During the experiment, the dates of initial flowering of M. micrantha and C. campestris and the dates of almost complete death of the aerial parts of the infected plants were recorded. On days 0, 10, 20, 30, 40, 50, 60, 100, and 120 after parasitization, eight uninfected and eight infected M. micrantha plants were selected at random and harvested. At each harvest, all the dead materials of both M. micrantha and C. campestris were carefully removed and weighed, while living parts were separated and handled as follows. Shoots of M. micrantha were separated into stems, leaves, and reproductive organs. Roots were soaked in tap water, washed, and separated carefully in running water over a 2-mm-mesh sieve. Stems, tendrils, and reproductive organs of C. campestris were carefully dissected from M. micrantha stems and leaves. After the number of leaves had been counted and the stem length determined, the total leaf area of each M. micrantha plant was measured using a CI-203 portable laser area meter. Plant materials were then dried at 70 °C until constant weight was achieved. On each harvest day, specific leaf area (SLA, the ratio of fresh leaf area to dry mass) and shoot:root dry weight ratio (S/R ratio) were determined. Relative growth rate (RGR, the rate of increase in total dry weight per plant per day), leaf area ratio (LAR, the ratio between total leaf area and total dry weight per plant), and unit leaf rate (ULR, the rate of dry weight production m–2 leaf area d–1) of M. micrantha plants were calculated according to Hunt and Parsons (1974).
Data analysis
All tests were carried out at P <0.05 significance level using SPSS (version 11.0). The differences in leaf number, stem length, leaf area, RGR, SLA, LAR, ULR, and the percentages of total biomass allocated to roots, stems, fruit and flowers, and leaves between the infected M. micrantha and controls were tested by Student's t-test for each harvest. One-way ANOVA was performed for total biomass of the infected plants, controls, and the infected system (host plus parasite). Means of the significant ANOVA effects were compared using Tukey post hoc comparisons.
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Results |
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During the experiment, the uninfected M. micrantha plants grew vigorously and developed normally, but the infected ones did not. On 19 October, 111 d after planting, the uninfected M. micrantha plants started to develop terminal inflorescences, 7 d thereafter they were in full bloom, and on 26 October they fruited. However, the infected plants did not flower at all in this experiment.
Cuscuta campestris significantly reduced the number of leaves per M. micrantha host from 20 to 100 DAP (Fig. 1a). On day 60 after parasitization, those infected had 12.9 leaves per plant, only 2.6% of the control, but there was no significant difference between the two treatments at the final harvest. From 40 to 100 DAP, there were significantly more younger leaves per plant (from the first to the fourth youngest fully expanded leaves) in controls than in infected M. micrantha (data not shown). They contributed to about 36.1–56.5% of the total leaf area in the control plant and 22.3–32.3% of that in the infected plants. At the end of the growing season, from 100 to 120 DAP, the uninfected M. micrantha showed a steep significant decline in the number of leaves. Cuscuta campestris also significantly reduced stem elongation of the infected plants from 30 DAP to the end of the experiment (Fig. 1b). A sharp decrease in the stem length in the infected plants occurred from 50 to 60 DAP, due to the dying off of the upper parts of the host shoots.
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Cuscuta campestris significantly reduced the total biomass of the infected plants compared with that of uninfected plants from 20 DAP to the end of the experiment (Fig. 1c). Moreover, the sum of the dry mass of the infected system (host plus parasite) was much less than that of the uninfected M. micrantha from 30 DAP onwards (P <0.01; data not shown). The effect of the parasite on the host could be divided into two phases. In the first phase, from 20 to 60 DAP, the effect became greater with time. By 60 DAP, the living dry matter of infected M. micrantha decreased to only 1.8% of the uninfected controls (Fig. 1c), and the dry mass of the infected system was only 11.5% of the uninfected controls. From 30 to 60 DAP, C. campestris grew vigorously with a lot of branching, and its total biomass increased from 0.8 g at 10 DAP to 19.9 g at 40 DAP (Fig. 1c). Then, from 40 to 60 DAP, concomitant with the decrease in the host biomass, the living biomass (including fruit) of the parasite also decreased. At 60 DAP, the dry weight (11.1 g) of the parasite was significantly greater than that (2.1 g) of its host. Cuscuta campestris started flowering 14 DAP and was in full bloom 8 d later. From 40 to 60 DAP, C. campestris flowered and fruited vigorously with about 67.4–85.7% of total biomass allocated to its fruit. Fruiting was complete just before the above-ground parts of the host started to die. Sixty-five days after parasitization, the aerial parts of the infected M. micrantha plants started to wither and they all died about 7 d later, but the parts up to the first node from the base of the stem remained alive.
In the second, recovery phase, from 60 to 120 DAP, new sprouts emerged from the first node at the base of the stem of the infected M. micrantha and the total biomass increased. By 100 DAP, the infected host had increased its biomass from 2.1 g at 60 DAP to 16.1 g. Nevertheless, the total biomass of infected M. micrantha remained significantly less than that of the uninfected plants. Furthermore, with the re-growth of the infected M. micrantha during this time, the remnant C. campestris also re-grew from 3.0 g at 100 DAP to 6.7 g at 120 DAP (Fig. 1c). Similar to the change in number of leaves, the dry weight of living tissues of the uninfected M. micrantha showed a steep decline at the end of the growing season, from 100 to 120 DAP.
Uninfected plants had greater RGR than the infected, and the difference became significant starting from 20 DAP (Fig. 1d). Moreover, the control also had greater RGR than the infected host plant and parasite together, in terms of shoot or shoot plus root (P <0.05; data not shown).
The S/R ratio of the infected M. micrantha was similar to that of the control up to 30 DAP, but the S/R ratio of the infected plants became significantly higher than that of the latter from 40 to 50 DAP (11.99±0.07 versus 7.44±0.78 at 40 DAP and 8.75±1.12 versus 6.05±0.79 at 50 DAP). At 60 DAP, with the dying of the aerial parts, the infected host had the minimum S/R ratio. Later, as the infected host re-grew in shoots, the S/R ratio increased but it remained significantly lower than that of the controls (data not shown).
The infection of C. campestris significantly increased biomass allocation to stems, while allocation to leaves and roots was decreased from 40 to 50 DAP (Table 1). At 60 DAP, the infected M. micrantha reached maximum allocation to roots and the minimum to stems and leaves. After 60 DAP, the parasite caused a significant increase in allocation to roots and leaves, but a decrease to stems.
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Infection by C. campestris significantly reduced leaf area of M. micrantha plants throughout the whole period of the experiment (Fig. 2a). At the end of the growing season, from 100 to 120 DAP, the uninfected M. micrantha showed a steep decline in leaf area (P <0.001). The SLA of the uninfected plants was significantly higher than that of the infected plants at 10 DAP and from 40 to 100 DAP (Fig. 2b).
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At 10 DAP and from 30 to 60 DAP, the LAR was significantly greater in the uninfected than in the infected plants; however, from 100 to 120 DAP, the opposite occurred (Fig. 2c). The ULR (Fig. 2d) had similar change patterns to the RGR (Fig. 1d) over time, and they were significantly correlated (r=0.969 in the infected group; r=0.956 in the control group). The leaf biomass change pattern (data not shown) was similar to those of leaf area (Fig. 2a), LAR (Fig. 2c), and ULR (Fig. 2d) in infected plants from 30 to 60 DAP.
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Discussion |
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Press et al. (1999)
indicated that the extent to which parasites compete with hosts for carbon and other nutrients depends on their relative sink strength and the degree of autotrophy of the parasite. Some studies have shown that the obligate parasite Cuscuta can form a strong sink to redirect the flow of host resources to itself (Jacob and Neumann, 1968; Wolswinkel, 1974; Fer, 1981; Jeschke et al., 1994a, b; Jeschke and Hilpert, 1997). This is supported by the present results that demonstrate that C. campestris severely inhibited both the growth and development of M. micrantha, even though one host plant was infected only by an individual parasite. The inhibitory effects of C. campestris on the biomass in M. micrantha hosts gradually increased in the first phase of the experiment, and the largest occurred at 60 DAP. Furthermore, C. campestris led to almost complete death of the aerial parts of the infected M. micrantha after about 72 d of parasitism, thus completely inhibiting flowering. It has been reported that Cuscuta delayed and reduced flowering in Vicia faba (Wolswinkel, 1974) and Ricinus communis (Jeschke and Hilpert, 1997).
Moreover, the present results indicate that dry mass of C. campestris plus host was less than that of uninfected M. micrantha. This is consistent with the relationship between Striga gesnerioides, S. hermonthica or S. asiatica and both C3 dicotyledonous species and C4 cereals, in which the depression of biomass accumulation in infected plants might be an order of magnitude greater than the biomass of the parasitic sink (Graves et al., 1989, 1990, 1992; Cechin and Press, 1993; Press, 1995a; Hibberd et al., 1996; Watling and Press, 1997). In a laboratory study of the parasitic association C. reflexa–Coleus blumei, the biomass of Cuscuta plus host was also less than that of uninfected Coleus, except at low N supply (Jeschke et al., 1997). In these cases, in addition to the parasite removing host resources, the rates of host photosynthesis were lower than those of the control. Thus, parasite biomass is generally a fraction of the observed difference between infected hosts and uninfected plants (Hibberd et al., 1998a). However, the study by Hibberd et al. (1998a, 1999) of the Orobanche cernua–tobacco association, showed that the parasite was able to modify the productivity of the tobacco host up to the resource capacity of the host, resulting in the overall productivity of the infected system being comparable to that of the uninfected. This led these researchers to suggest that the response of the host to infection could be explained by simple source–sink interactions, in that the difference in biomass between infected and uninfected tobacco could be accounted for directly by diversion of dry matter to the parasite, and the productivity of the infected system was maintained by sustained production of leaf area (a greater LAR), increased specific leaf area, and delayed senescence.
With the vegetative growth of its host, C. campestris increased in dry mass with time from 10 to 40 DAP; then it decreased from 40 to 60 DAP in parallel with the decreasing growth of its M. micrantha host. Similar trends have been observed for R. communis and C. blumei (Jeschke and Hilpert, 1996, 1997; Jeschke et al., 1997) and O. cernua and tobacco (Hibberd et al., 1998a, 1999).
In the present study, C. campestris completed its fruiting before almost all the above-ground parts of its host died. This showed that the life cycle of C. campestris is well adapted to the resource availability of its hosts, which is similar to what had been found by Jeschke et al. (1997). Therefore, it seemed that C. campestris could ‘sense’ the developmental status of its host and timely regulate its growth and development accordingly. This indicates a synchronicity between the parasite development and its host. The chemical and physiological mechanisms responsible for this phenomenon need to be studied in future.
From 40 to 50 DAP, the S/R ratio of the infected host increased significantly in the present study. Jeschke et al. (1994b, 1997) have reported similar results in other parasitic angiosperm associations, such as C. reflexa–Lupinus albus and C. reflexa–Coleus blumei with a high N supply. Such increases may be due to a strong competition of the parasite with the host root (Jeschke et al., 1997). However, in root parasites, substantial changes in the S/R ratio in favour of the root have been reported (Ernst, 1986; ter Borg, 1986; Graves et al., 1989, 1990; El-Ghamrawy and Neumann 1991; Cechin and Press, 1993, 1994; Graves, 1995; Barker et al., 1996). Thus, the different types of parasitism, the former being a stem parasite and the latter a root parasite, may have caused this difference in the S/R ratio. Another possibility is that, in the present study, when the upper parts of M. micrantha were infected by C. campestris, M. micrantha responded by allocating more resources to shoot growth.
In the present study, the highest biomass allocation to roots and the smallest to leaves and stems in the infected hosts at 60 DAP must be due to the death of their stems and leaves at this time. Thus, the root system of the infected M. micrantha was not adversely affected by the parasite as much as the above-ground parts were. With the re-growing of the infected M. micrantha after 60 DAP, the infected M. micrantha increased resource allocation to the above-ground parts, with more to leaves than to stems, and decreased allocation to roots. Such a resource allocation strategy would facilitate the parasitized re-growing M. micrantha to increase leaf area in order to produce more photosynthetates and so increase its survival and regain its competitive ability.
The present results showed the leaf area of the infected M. micrantha was significantly lower than that of the control throughout the growing season. This might be due either to the inhibition in leaf expansion or to the reduction in the number of leaves or both. This is consistent with the observation on Sorghum bicolor infected by Striga hermonthica and S. asiatica (Watling and Press, 1997). More interestingly, in the present study, the decreases in leaf area, LAR, and SLA only became significant at 10 DAP. Also, at this time the allocation to leaves was significantly higher in the infected than in the control, but not to roots and stems. These indicate that C. campestris is very aggressive, and its negative effects on M. micrantha are very fast upon infection and the leaves of M. micrantha are most sensitive to infection. In response, infected M. micrantha plants allocated more resources to leaves. However, such increased allocation to leaves did not increase the leaf area and LAR, but it occurred as the SLA decreased. This might be caused by inhibition in leaf expansion or reduced remobilization of reserves from the infected leaves or both at the beginning of the infection. From 40 to 100 DAP, the SLA of the uninfected plants was significantly higher than that of the infected plants. This accompanied the significantly reduced number of new leaves and the proportion of new to old leaf areas. Therefore, during this period, the smaller SLA of the infected plants might also be caused by the inhibited initiation of new leaves. This is in contrast to the fact that there was no difference in the SLA between infected and uninfected tobacco plants by O. cernua by day 16 after parasitization, but by day 49 it was higher in the infected plants than in the control (Hibberd et al., 1998a).
The present results show that from 10 to 60 DAP, leaf area, LAR, and allocation to leaf biomass decreased and reached their minima, and the differences in these parameters as well as in SLA between the infected and the uninfected plants reached their maxima. Thus, the infected plants allocated fewer and fewer resources for leaf production than did the uninfected. Furthermore, from 30 to 50 DAP, allocation to leaves was significantly less in the infected hosts; allocation to stems increased, and significantly so from 40 to 50 DAP. Also, from 40 to 50 DAP, allocation to roots was significantly less in the infected plants. These findings indicate that, during this period of time, a relatively smaller and smaller leaf area had to support more and more non-photosynthetic biomass. This must have eventually exceeded the support capacity of the leaves and, at 72 DAP, the aerial parts of the infected M. micrantha plants died. This compares with the results observed in Striga–host associations in which the parasite did not cause significant changes in dry mass partitioning between photosynthetic and non-photosynthetic tissues in their hosts (Press and Stewart, 1987; Cechin and Press, 1993).
The RGR was lower in infected M. micrantha than in the controls in the present study. This is similar to that reported in sorghum infected by S. hermonthica (Cechin and Press, 1993) and tomato infected by Orobanche aegyptiaca (Barker et al., 1996). However, a slight stimulation of the growth of Vicia faba infected by O. crenata (ter Borg and van Ast, 1991) and early stimulation of the RGR of infected tomato by O. aegyptiaca (Barker et al., 1996) have been reported. The LAR represents the size of the photosynthetic surface area relative to the non-photosynthetic biomass, while the ULR indicates the photosynthesis efficiency that is related to rates of photosynthesis and respiration (Barker et al., 1996). Thus, a drop in LAR and ULR may be the cause for the drop in RGR. The present results show that, among the changing patterns of leaf parameters, leaf biomass, leaf area, LAR, and ULR over time, the pattern of the ULR was most like that of the RGR and was highly correlated with it. Thus, ULR might be the main factor contributing to the lower RGR of the infected M. micrantha.
In summary, the results indicate that once a C. campestris–M. micrantha association has been established, the parasite could severely restrain the growth of M. micrantha, inhibit its flowering, and even result in almost complete death of its aerial parts during a growing season. Therefore, C. campestris has great potential to control M. micrantha effectively. However, the use of C. campestris to control M. micrantha under field conditions needs to be studied in order to develop application methods, understand its effectiveness, and find out its effects on the M. micrantha community structure and function, including plant species composition, species diversity, and community succession. Nevertheless, the application of this parasitic relationship could help us achieve the objective, ‘biological control of weeds by weeds’, and also provide a new strategy for developing knowledge and techniques in the biological control of exotic species.
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Acknowledgements |
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We thank Chris Parker for his research guidance, Chris Parker, Yi Zhu Chen and Sheng Bin Chiu for their constructive comments on the manuscript. This work was supported by the National Natural Science Foundation of China (30370248, 30470345) and the National Natural Science Foundation of Guangdong Province, China (021536).
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Footnotes |
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Abbreviations: DAP, days after parasitization; LAR, leaf area ratio; RGR, relative growth rate; SLA, specific leaf area; S/R ratio, shoot:root dry weight ratio; ULR, unit leaf rate.
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References |
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