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Effects of simulated herbivory and resource availability on the invasive plant, Alternanthera philoxeroides in different habitats
Biological Control 48 (2009) 287–293
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Biological Control journal homepage: www.elsevier.com/locate/ybcon
Effects of simulated herbivory and resource availability on the invasive plant, Alternanthera philoxeroides in different habitats Yan Sun a,b, Jianqing Ding a,*, Mingxun Ren a a b
Wuhan Botanical Institute/Wuhan Botanical Garden, Chinese Academy of Sciences, Wuhan, Hubei 430074, China Graduate School of the Chinese Academy of Sciences, Beijing 100049, China
a r t i c l e
i n f o
Article history: Received 26 August 2008 Accepted 3 December 2008 Available online 24 December 2008 Keywords: Alligator weed Alternanthera philoxeroides Tolerance Compensatory response Simulated herbivory Fertilization Habitat
a b s t r a c t In biological control programs, the insect natural enemy’s ability to suppress the plant invader may be affected by abiotic factors, such as resource availability, that can influence plant growth and reproduction. Understanding plant tolerance to herbivory under different environmental conditions will help to improve biocontrol efficacy. The invasive alligator weed (Alternanthera philoxeroides) has been successfully controlled by natural enemies in many aquatic habitats but not in terrestrial environments worldwide. This study examined the effects of different levels of simulated leaf herbivory on the growth of alligator weed at two levels of fertilization and three levels of soil moisture (aquatic, semi-aquatic, and terrestrial habitats). Increasing levels of simulated (manual) defoliation generally caused decreases in total biomass in all habitats. However, the plant appeared to respond differently to high levels of herbivory in the three habitats. Terrestrial plants showed the highest below–above ground mass ratio (R/S), indicating the plant is more tolerant to herbivory in terrestrial habitats than in aquatic habitats. The unfertilized treatment exhibited greater tolerance than the fertilized treatment in the terrestrial habitat at the first stage of this experiment (day 15), but fertilizer appears not to have influenced tolerance at the middle and last stages of the experiment. No such difference was found in semi-aquatic and aquatic habitats. These findings suggest that plant tolerance is affected by habitats and soil nutrients and this relationship could influence the biological control outcome. Plant compensatory response to herbivory under different environmental conditions should, therefore, be carefully considered when planning to use biological control in management programs against invasive plants. Ó 2008 Elsevier Inc. All rights reserved.
1. Introduction Invasive species are a serious threat to natural ecosystems and often cause economic losses in agriculture (Mack et al., 2000). Control of invasive plant species can be achieved through mechanical, chemical or biological control. Since many invasive plant species grow in different habitats, understanding their response to different environmental factors will help to improve control efficacy. In biological control programs, the insect natural enemy’s ability to suppress the plant invader may be affected by abiotic factors, such as resource availability (water, nutrients, etc.), that can influence the growth and reproduction of invasive plant species (Davis et al., 2000; Dukes and Mooney, 1999). Plants may employ different strategies to defend against herbivory (Strauss and Agrawal, 1999). The two main forms of plant response to herbivory are tolerance (i.e., compensatory growth) and resistance (i.e., physical and chemical defenses) (Gadd et al., 2001; Rosenthal and Kotanen, 1994). Tolerance is the ability of a * Corresponding author. Fax: +86 27 87510251. E-mail address: [email protected] (J. Ding). 1049-9644/$ - see front matter Ó 2008 Elsevier Inc. All rights reserved. doi:10.1016/j.biocontrol.2008.12.002
plant to withstand and survive a fixed amount of herbivore damage without a corresponding reduction in fitness (McNaughton, 1983; Paige and Whitham, 1987). Compensatory growth following herbivory is influenced by environmental resource availability (Gadd et al., 2001; Rosenthal and Kotanen, 1994). Several hypotheses have been proposed to explain the effects of resource availability on tolerance. The current prevailing hypotheses include the compensatory continuum hypothesis (CCH), the growth rate model (GRM), and the limiting resource model (LRM). CCH predicts that tolerance to herbivory should be greater in high-resource and low-stress conditions (Fornoni et al., 2003; Hawkes and Sullivan, 2001; Strauss and Agrawal, 1999). On the contrary, GRM predicts that tolerance to herbivory should be greater in more stressful conditions (Alward and Joern, 1993; Hawkes and Sullivan, 2001). LRM, a recently introduced model, is more flexible than the CCH or GRM because it allows for predictions of tolerance by identifying focal resource (Wise and Abrahamson,2005, 2007). However, there are few studies documenting the invasive plant tolerance to herbivory under different resource conditions (but see Rogers and Siemann, 2002). Alligator weed, Alternanthera philoxeroides (Martius) Grisebach (Amaranthaceae), native to South America, is presently distributed
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widely in temperate and subtropical areas throughout the world (Julien et al., 1995). Alternanthera philoxeroides is a stoloniferous, rhizomatous, and perennial herbaceous plant. Prolific asexual reproduction from apical stem buds and auxiliary stem and root buds (Julien et al., 1995) allows it to rapidly establish large populations (Li and Ye, 2006). Viable seeds are not produced in introduced ranges in Australia, USA and China (Ma et al., 2003). The plant grows in both terrestrial and aquatic environments. Terrestrial forms have smaller and slightly hollow stems, but aquatic forms have larger hollow stems that promote buoyancy (Julien et al., 1992). Alternanthera philoxeroides was first reported near Shanghai, China in 1892 and has been cultivated as pig food since the 1950s (Zhang et al., 2006). Subsequently it has invaded large areas south of the Yellow River Basin (Zhang et al., 2006) and is considered one of the 16 most important invasive species in China (Li and Xie, 2002). It blocks drainage and irrigation channels, where it causes problems on agricultural land, and with fisheries, irrigation, and natural ecosystems (Spencer and Coulson, 1976). Beginning in the late 1960s, a leaf beetle, Agasicles hygrophila Selman and Vogt (Chrysomelidae: Alticinae), from Argentina has been used as a biological control agent worldwide (Buckingham et al., 1983; Sainty et al., 1997). Agasicles hygrophila was first introduced for biocontrol in China in 1986, and preliminary surveys indicated successful suppression of A. philoxeroides in aquatic environments but not in terrestrial habitats (Ma et al., 2003). More efforts are currently focused on screening natural enemies that can effectively control the plant in terrestrial habitats (A. Sosa, personal communication). However, little information is available on the plant response to differing resources and habitats, when subjected to herbivory. Such knowledge will be critical to improve biological control efficacy under different environmental conditions. Simulated herbivory (e.g., clipping or hole-punching) is a technique often used as a substitute for actual herbivory in ecological studies of insect–plant interactions (Schooler et al., 2006), because it offers a precise control on the amount and timing of plant damage (Baldwin, 1990). Previous studies have shown that A. philoxeroides biomass responds similarly to simulated and actual herbivory (Schooler et al., 2006). Here, we investigate A. philoxeroides response to simulated herbivory under various fertilization and soil moisture environments. We hypothesized that (i) A. philoxeroides would exhibit higher herbivory tolerance in terrestrial habitat than in semi-aquatic or aquatic habitats; (ii) A. philoxeroides would have higher tolerance in nutrient-poor environments.
Table 1 Experimental treatment design. All potted A. philoxeroides plants were randomly assigned to treatment combinations in a full-factorial experimental design (n = 3 moisture treatments 2 fertilized treatments 5 herbivory treatments 20 replicates 3 sampling periods = 1800). An additional 600 plants were planted, but not sampled. Soil moisture treatments (M)
Fertilized treatments (N)
Herbivory treatments (H)
M0 6 20% Terrestrial habitat M1 = 40–45% Semi-aquatic habitat M2 = 100% Aquatic habitat
N0 = 0 g N m 2 Unfertilized N1 = 20 g N m 2 Fertilized
H0 = Control H1 = 10% leaf H2 = 20% leaf H3 = 50% leaf H4 = 90% leaf
removal removal removal removal
Herbivory was simulated by use of a steel hole punch. At the start of the study, 20 A. philoxeroides plants from five different locations in Wuhan were collected to measure the holes produced by herbivores, most of which were made by the introduced A. hygrophila and a native tortoise beetle, Cassida piperata Hope (Coleoptera: Chrysomelidae), on 10 leaves from each plant. The feeding holes were 2–7 mm in diameter for each beetle, which supports the use of a 6-mm diameter punch to simulate herbivory. The punch removed a portion of the leaf while leaving the mid-vein intact (Schooler et al., 2006). Leaf herbivory was simulated three times (31 August, 24 September, and 15 October) during the experiment to mimic repeated herbivore pressure. Plants assigned to simulated herbivory treatments were initially subjected to 10% leaf removal (H1), 20% leaf removal (H2), 50% leaf removal (H3), or 90% leaf removal (H4) (Table 1). The numbers of hole punches on each leaf were determined by the leaf area size. Using the Gravimetric method (Wu et al., 2007), three soil moisture levels were simulated: 620% (terrestrial, M0), 40–45% (semiaquatic, M1), and 100% (aquatic, M2) (Table 1). These values represent the different habitats where A. philoxeroides occurs. Soil moisture content was monitored and the pots were watered as necessary. From each pot, 6–15 g of soil was weighed before and after drying in an oven for 24 h at 104 °C. Plants assigned to fertilization treatments received either 0 g N m 2 (N0) or 20 g N m 2 (N1) during week two (starting 13 September) (Table 1). Slow release fertilizer (N:P:K = 15:15:15) was added as ammonium nitrate powder. 2.2. Data collection and statistical analysis
2. Materials and methods 2.1. Experimental design The experiment was conducted in a greenhouse at the Wuhan Botanical Institute/Wuhan Botanical Garden from July to October 2007. Average temperatures in the greenhouse were between 30–35 °C from July to September and 15–25 °C during October. Hundreds of A. philoxeroides plants were propagated from stems collected at Yuemachang, Wuhan on 31 July 2007. Stem cuttings (3000) that were 4–5 cm in length and each with one node were planted vertically in 43 32 11 cm plastic boxes. When the new shoots reached a height of approximately 5 cm (about 27 days after planting), the seedlings were repotted. Over 90% of the cuttings survived and the smallest 10% of plants were discarded. A total of 2400 plants were transplanted into 150 plastic containers (43 32 11 cm) on 1 September 2007. Each container had 16 plants, with each plant placed approximately 10 cm from its neighbors. Treatments were randomly assigned to each box in a full-factorial experimental design with five levels of simulated herbivory, two levels of fertilized addition, and three levels of soil moisture content (Table 1). Each treatment was replicated 20 times.
Random subsets of 20 plants per treatment combination (n = 600) were destructively sampled on three occasions: 15 September 2007 (day 15), 30 September 2007 (day 30), and 30 October 2007 (day 60). At each occasion the mass of roots, stems, and leaves, and the lengths of roots and stems were measured. From these measurements, total biomass and the ratio of root: shoot mass were calculated. Three-factor analysis of variance (ANOVA) was performed to analyze the effects of the range of environmental resource conditions (soil moisture, fertilization, and herbivory) on the biomass, root mass, stem mass, ratio of root: shoot mass, and growth rate of root length and of stem height. All data were analyzed using SPSS 13.0 for windows (SPSS Inc.) 3. Results 3.1. Total biomass Alternanthera philoxeroides total biomass was significantly affected by simulated herbivory and fertilization (Table 2). Increasing levels of simulated herbivory generally caused decreases in total biomass at all soil moisture levels (Fig. 1). At the first stage
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Table 2 Three-way analysis of variance tables comparing total biomass and root:shoot mass ratio for A. philoxeroides. The experimental treatments: H, simulated herbivory; N, fertilizer addition; M, soil moisture content at three sampling periods. Source
df
Total biomass
Root:shoot mass
Day 15
H N M HN HM NM HNM
4 1 2 4 8 2 8
Day 30
Day 60
Day 15
Day 30
Day 60
F
P
F
P
F
P
F
P
F
P
F
P
197.154 380.682 84.188 15.644 6.890 3.858 9.094
****
114.114 129.423 8.586 6.570 8.402 9.987 0.927
****
76.680 243.937 2.313 16.457 3.058 3.112 3.050
****
9.381 0.005 27.547 1.812 9.594 2.494 0.0694
****
46.230 11.232 5.951 0.849 2.189 0.390 1.379
****
28.150 0.348 79.041 1.309 24.196 11.740 0.905
****
**** **** **** **** * ****
**** **** **** **** ****
0.496
****
0.104 **** ** * **
0.944 ****
0.130 ****
0.086 0.696
*** **
0.496 *
0.677 0.210
0.556 ****
0.271 **** ****
0.515
*
P 6 0.05. P 6 0.01. P 6 0.001. **** P 6 0.0001. **
***
of this experiment (day 15, Fig. 1A), the difference in biomass between herbivory treatments (H0–H4) in the unfertilized group was smaller than that in the fertilized group, indicating a higher compensation capacity in unfertilized plants in a terrestrial habitat. However, there were no such differences between the two fertilized treatments in semi-aquatic and aquatic habitats. The biomass of the middle level of herbivory treatments (H3) at the
end of the experiment (day 60, Fig. 1C) was smallest in all of the three habitats. 3.2. Root:shoot (R/S) biomass ratio Alternanthera philoxeroides R/S ratio was significantly affected by simulated herbivory and soil moisture (Table 2). When plants
Fig. 1. Mean total biomass (g) for A. philoxeroides at three sampling dates (A: day 15, B: day 30, C: day 60) in full-factorial combination of five levels of simulated herbivory (H), two levels of fertilizer addition (N), and three levels of soil moisture content (M) treatments.
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suffered the highest level of simulated herbivory (H4), their R/S ratio in semi-aquatic and aquatic habitats increased significantly in the short term (Fig. 2B) but then decreased at the end of the experiment (Fig. 2C); however, the R/S ratio in the terrestrial habitat was maintained at a high level during the entire experiment (Fig. 2). At the end of the experiment (day 60), the R/S ratio of terrestrial habitat plants was significantly higher than semi-aquatic and aquatic habitats plants in the highest level of simulated herbivory treatment (H4), whereas the total biomass was not influenced when they grew in the same habitat, indicating more biomass was allocated to the below-ground portion of the plant in the terrestrial habitat. The R/S ratio increased more rapidly in the terrestrial habitat (M0) but very slowly in the aquatic habitat (M2) (Fig. 3 and Table 2). There was no significant effect of fertilizer on R/S ratio during the first or third sampling periods. However, fertilizer treatments significantly influenced R/S ratio during the second sampling period (Table 2).
Fig. 3. Mean root:shoot mass ratio for A. philoxeroides at three levels of soil moisture content (M) treatments during the experiment.
3.3. Growth rate Soil moisture treatments influenced root growth significantly. The root growth was slower in the aquatic habitat than in the terrestrial habitat. Herbivory and fertilizer treatments had no effect
on root growth (Table 3). The average root length growth rate per day (RLGR) (in 60 days) was higher in the terrestrial habitat than in the aquatic and semi-aquatic habitats (Fig. 4A). There was a significant interaction between herbivory and soil moisture on root
Fig. 2. Mean root:shoot mass ratio for A. philoxeroides at three sampling dates (A: day 15, B: day 30, C: day 60) in full-factorial combination of five levels of simulated herbivory (H), two levels of fertilizer addition (N), and three levels of soil moisture content (M) treatments.
Y. Sun et al. / Biological Control 48 (2009) 287–293 Table 3 Three-way analysis of variance tables comparing average root length growth rate and stem height growth rate for A. philoxeroides. The experimental treatments: H, simulated herbivory; N, fertilizer addition; M, soil moisture content during the entire experiment (60 days). Source
H N M HN HM NM HNM * **
df
4 1 2 4 8 2 8
Root length growth rate
Stem height growth rate
F
P
F
P
2.210 1.385 18.151 0.684 2.580 1.672 1.283
0.072 0.242
1.469 5.734 70.011 3.872 2.986 2.411 2.710
0.235
****
0.605 *
0.192 0.259
**** **** ****
0.055 0.053 **
P 6 0.05. P 6 0.01. P 6 0.0001.
****
growth in the terrestrial habitat (Table 3): the RLGR was lower in the second level herbivory treatment (H2) but increased significantly in the highest level herbivory treatment, when fertilized. Soil moisture and fertilization significantly influenced stem growth (Table 3 and Fig. 4B). The averaged stem height growth rate (STGR) was significantly higher in the aquatic habitat than in the terrestrial habitat. Fertilization significantly increased the stem growth in all the three habitats. There were no differences between the simulated herbivory level treatments; however, the interaction of simulated herbivory levels and fertilization significantly affected the STGR (Table 3). Plants that suffered the highest simulated herbivory level showed lower STGR when unfertilized, but when fertilized, their stems grew more rapidly. 4. Discussion By repeated destructive samplings, this study tested how a herbaceous plant recovered after simulated herbivory under different
291
environmental conditions. The results highlighted several important aspects which had not been addressed in previous studies. Here, we present two major findings: (i) A. philoxeroides had a higher tolerance to herbivory in terrestrial than in semi-aquatic and aquatic habitats, as indicated by higher root compensation in terrestrial habitats after simulated herbivory; (ii) the plant had higher tolerance under poor resource conditions, i.e., compensation capacity in the unfertilized treatment was higher than in the fertilized treatment. Simulated herbivory caused a decline in total biomass in all habitats. However, in general, A. philoxeroides appeared to respond differently to high levels of herbivory in the three habitats, with terrestrial plants showing the highest R/S biomass ratio. This indicates that the plant compensation capacity in terrestrial habitat is higher than that in other two habitats. The weed usually experiences more disturbance (e.g., natural enemies, fire, human-activities, etc.), in terrestrial habitats than aquatic habitats (Ma et al., 2003). Phenotypic adaptation may, therefore, explain the different compensation capacity between terrestrial and aquatic forms of A. philoxeroides. Moreover, above ground damage of terrestrial A. philoxeroides would create a nutrient sink which would drain nutrients from other parts of the plant, primarily from root tissues (Schooler et al., 2007). Interestingly, at the end of the experiment the plant’s total biomass and RLGR of the medium level herbivory treatments (H3) were the smallest in all the three habitats. This indicates that the compensation of A. philoxeroides may be influenced by damage level. When plants were damaged at the medium level (H3), the compensatory regrowth was lowest. Some unexpected trends were observed at day 30. Herbivory affected R/S ratio significantly in the aquatic and semi-aquatic habitats. Responses to herbivory may depend on the intrinsic growth rate of the plant species (Houle and Simard, 1996), the timing, type, and extent of herbivory (McNaughton, 1983; Rosenthal and Kotanen, 1994) and morphological or physiological traits that allow the plant to replace lost biomass (Tiffin, 2000). The particular
Fig. 4. Mean root length growth rate mass (A) and stem height growth rate mass (B) for A. philoxeroides at day 60 in full-factorial combination of three with five levels of simulated herbivory (H), two levels of fertilizer addition (N), and three levels of soil moisture content (M) treatments.
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time in the life cycle at which herbivory takes place may also play an important role (Prins et al., 1989). Therefore, these exceptions could have occurred because the second sampling period was only 5 days after simulated herbivory. In the case of R/S ratio, all plant roots were stimulated to grow quickly, but only the terrestrial A. philoxeroides could maintain a high R/S ratio at the highest level of simulated herbivory over the duration of the experiment. These findings indicate that A. philoxeroides demonstrates compensatory root growth after severe leaf herbivory, but that this response is more persistent in terrestrial than aquatic or semi-aquatic populations. For the second hypothesis, that A. philoxeroides would demonstrate greater tolerance in the nutrient-poor soil, we found that herbivory induced greater tolerance in unfertilized treatments than fertilized treatments in the terrestrial habitat at the first stage of the experiment (day 15), but fertilizer appeared not to influence tolerance at the middle and last stages of the experiment. Fertilizer was applied only once and may have been depleted over time. Future studies should use a gradient of fertilizer, applied at regular intervals throughout the experiment. Fertilizer affected SHGR significantly but had no effect on RLGR (Fig. 4A), implying different resource allocation strategies between above- and below-ground biomass, with different nutritional status. When the soil is nutrient poor, the damaged plant may allocate more nutrients to root growth to adapt to stressful environments, but allocates more resources to grow stems under favorable (nutrient-rich) conditions. Therefore, the results support the predictions of GRM: the weed is more tolerant in nutrient-poor soils. The results indicate a higher tolerance to herbivory by A. philoxeroides in terrestrial habitats than in aquatic habitats. Although it is known that the flea beetle, A. hygrophila is unable to control A. philoxeroides in terrestrial habitats due to low pupal survival on the solid-narrow hollow stems (Ma et al., 2003), the results may provide a supplementary explanation for the failure. The flea beetle has been considered an aquatic insect (Julien et al., 1995), however, its populations have been recently found on terrestrial forms of A. philoxeroides in Hubei Province, China (J. Ding, unpublished data). This study also indicates that biological control using leaf feeders would be more efficient in nutrient-rich conditions, as A. philoxeroides showed increased tolerance in nutrient-poor conditions than in nutrient-rich conditions. Therefore, the compensatory response of A. philoxeroides to other insect defoliators such as the alligator weed thrips, Amynothrips andersoni O’Neill (Thysanaptera: Phlaeothripidae) under different environmental conditions should be carefully considered in biological control programs. Local adaptability and phenotypic plasticity allow many exotic plant species to be highly invasive in variable environmental conditions (Ghalambor et al., 2007; Richards et al., 2006). Given the low success rate of classical biological control, i.e., only 33% released agents have successfully controlled target weeds (McFadyen, 1998), identifying the abiotic factors that affect the insect natural enemy’s ability to suppress the plant invader is critical to improve control efficacy. This study suggests that resource availability (water, nutrients, etc.) that often influences the growth and reproduction of invasive plant species may play an important role in biological control through regulating the plant tolerance to herbivory. Understanding mechanisms in plant invader compensation under different environmental conditions is important for improving management efficiency. Acknowledgments We thank Hongjun Dai, Yi Wang, Wenfeng Guo, Xinmin Lu, Wei Huang, Yangzhou Wang, Kai Wu, and Jialiang Zhang for their field and lab assistance. The comments of Michael J. Wise, Heinz Müller-Schärer, Ashley K. Baldridge, Matthew A. Barnes, John
Hoffmann, and two anonymous reviewers improved earlier versions of this paper. This work was funded by the Knowledge Innovation Program of the Chinese Academy of Sciences and the National Science Foundation of China (30871650) while preparing this manuscript. References Alward, R.D., Joern, A., 1993. Plasticity and overcompensation in grass responses to herbivory. Oecologia (Berlin) 95, 358–364. Baldwin, I.T., 1990. Herbivory simulations in ecological research. Trends in Ecology & Evolution 5, 91–93. Buckingham, G.R., Boucias, D., Theriot, R.F., 1983. Reintroduction of the alligator weed flea beetle (Agasicles hygrophila Selman and Vogt) into the United States from Argentina. Journal of Aquatic Plant Management 21, 101–102. Davis, M.A., Grime, J.P., Thompsom, K., 2000. Fluctuating resources in plant communities: a general theory of invasibility. Journal of Ecology 88, 528–534. Dukes, J.S., Mooney, H.A., 1999. Does global change increase the success of biological invaders? 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Biological Control journal homepage: www.elsevier.com/locate/ybcon
Effects of simulated herbivory and resource availability on the invasive plant, Alternanthera philoxeroides in different habitats Yan Sun a,b, Jianqing Ding a,*, Mingxun Ren a a b
Wuhan Botanical Institute/Wuhan Botanical Garden, Chinese Academy of Sciences, Wuhan, Hubei 430074, China Graduate School of the Chinese Academy of Sciences, Beijing 100049, China
a r t i c l e
i n f o
Article history: Received 26 August 2008 Accepted 3 December 2008 Available online 24 December 2008 Keywords: Alligator weed Alternanthera philoxeroides Tolerance Compensatory response Simulated herbivory Fertilization Habitat
a b s t r a c t In biological control programs, the insect natural enemy’s ability to suppress the plant invader may be affected by abiotic factors, such as resource availability, that can influence plant growth and reproduction. Understanding plant tolerance to herbivory under different environmental conditions will help to improve biocontrol efficacy. The invasive alligator weed (Alternanthera philoxeroides) has been successfully controlled by natural enemies in many aquatic habitats but not in terrestrial environments worldwide. This study examined the effects of different levels of simulated leaf herbivory on the growth of alligator weed at two levels of fertilization and three levels of soil moisture (aquatic, semi-aquatic, and terrestrial habitats). Increasing levels of simulated (manual) defoliation generally caused decreases in total biomass in all habitats. However, the plant appeared to respond differently to high levels of herbivory in the three habitats. Terrestrial plants showed the highest below–above ground mass ratio (R/S), indicating the plant is more tolerant to herbivory in terrestrial habitats than in aquatic habitats. The unfertilized treatment exhibited greater tolerance than the fertilized treatment in the terrestrial habitat at the first stage of this experiment (day 15), but fertilizer appears not to have influenced tolerance at the middle and last stages of the experiment. No such difference was found in semi-aquatic and aquatic habitats. These findings suggest that plant tolerance is affected by habitats and soil nutrients and this relationship could influence the biological control outcome. Plant compensatory response to herbivory under different environmental conditions should, therefore, be carefully considered when planning to use biological control in management programs against invasive plants. Ó 2008 Elsevier Inc. All rights reserved.
1. Introduction Invasive species are a serious threat to natural ecosystems and often cause economic losses in agriculture (Mack et al., 2000). Control of invasive plant species can be achieved through mechanical, chemical or biological control. Since many invasive plant species grow in different habitats, understanding their response to different environmental factors will help to improve control efficacy. In biological control programs, the insect natural enemy’s ability to suppress the plant invader may be affected by abiotic factors, such as resource availability (water, nutrients, etc.), that can influence the growth and reproduction of invasive plant species (Davis et al., 2000; Dukes and Mooney, 1999). Plants may employ different strategies to defend against herbivory (Strauss and Agrawal, 1999). The two main forms of plant response to herbivory are tolerance (i.e., compensatory growth) and resistance (i.e., physical and chemical defenses) (Gadd et al., 2001; Rosenthal and Kotanen, 1994). Tolerance is the ability of a * Corresponding author. Fax: +86 27 87510251. E-mail address: [email protected] (J. Ding). 1049-9644/$ - see front matter Ó 2008 Elsevier Inc. All rights reserved. doi:10.1016/j.biocontrol.2008.12.002
plant to withstand and survive a fixed amount of herbivore damage without a corresponding reduction in fitness (McNaughton, 1983; Paige and Whitham, 1987). Compensatory growth following herbivory is influenced by environmental resource availability (Gadd et al., 2001; Rosenthal and Kotanen, 1994). Several hypotheses have been proposed to explain the effects of resource availability on tolerance. The current prevailing hypotheses include the compensatory continuum hypothesis (CCH), the growth rate model (GRM), and the limiting resource model (LRM). CCH predicts that tolerance to herbivory should be greater in high-resource and low-stress conditions (Fornoni et al., 2003; Hawkes and Sullivan, 2001; Strauss and Agrawal, 1999). On the contrary, GRM predicts that tolerance to herbivory should be greater in more stressful conditions (Alward and Joern, 1993; Hawkes and Sullivan, 2001). LRM, a recently introduced model, is more flexible than the CCH or GRM because it allows for predictions of tolerance by identifying focal resource (Wise and Abrahamson,2005, 2007). However, there are few studies documenting the invasive plant tolerance to herbivory under different resource conditions (but see Rogers and Siemann, 2002). Alligator weed, Alternanthera philoxeroides (Martius) Grisebach (Amaranthaceae), native to South America, is presently distributed
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widely in temperate and subtropical areas throughout the world (Julien et al., 1995). Alternanthera philoxeroides is a stoloniferous, rhizomatous, and perennial herbaceous plant. Prolific asexual reproduction from apical stem buds and auxiliary stem and root buds (Julien et al., 1995) allows it to rapidly establish large populations (Li and Ye, 2006). Viable seeds are not produced in introduced ranges in Australia, USA and China (Ma et al., 2003). The plant grows in both terrestrial and aquatic environments. Terrestrial forms have smaller and slightly hollow stems, but aquatic forms have larger hollow stems that promote buoyancy (Julien et al., 1992). Alternanthera philoxeroides was first reported near Shanghai, China in 1892 and has been cultivated as pig food since the 1950s (Zhang et al., 2006). Subsequently it has invaded large areas south of the Yellow River Basin (Zhang et al., 2006) and is considered one of the 16 most important invasive species in China (Li and Xie, 2002). It blocks drainage and irrigation channels, where it causes problems on agricultural land, and with fisheries, irrigation, and natural ecosystems (Spencer and Coulson, 1976). Beginning in the late 1960s, a leaf beetle, Agasicles hygrophila Selman and Vogt (Chrysomelidae: Alticinae), from Argentina has been used as a biological control agent worldwide (Buckingham et al., 1983; Sainty et al., 1997). Agasicles hygrophila was first introduced for biocontrol in China in 1986, and preliminary surveys indicated successful suppression of A. philoxeroides in aquatic environments but not in terrestrial habitats (Ma et al., 2003). More efforts are currently focused on screening natural enemies that can effectively control the plant in terrestrial habitats (A. Sosa, personal communication). However, little information is available on the plant response to differing resources and habitats, when subjected to herbivory. Such knowledge will be critical to improve biological control efficacy under different environmental conditions. Simulated herbivory (e.g., clipping or hole-punching) is a technique often used as a substitute for actual herbivory in ecological studies of insect–plant interactions (Schooler et al., 2006), because it offers a precise control on the amount and timing of plant damage (Baldwin, 1990). Previous studies have shown that A. philoxeroides biomass responds similarly to simulated and actual herbivory (Schooler et al., 2006). Here, we investigate A. philoxeroides response to simulated herbivory under various fertilization and soil moisture environments. We hypothesized that (i) A. philoxeroides would exhibit higher herbivory tolerance in terrestrial habitat than in semi-aquatic or aquatic habitats; (ii) A. philoxeroides would have higher tolerance in nutrient-poor environments.
Table 1 Experimental treatment design. All potted A. philoxeroides plants were randomly assigned to treatment combinations in a full-factorial experimental design (n = 3 moisture treatments 2 fertilized treatments 5 herbivory treatments 20 replicates 3 sampling periods = 1800). An additional 600 plants were planted, but not sampled. Soil moisture treatments (M)
Fertilized treatments (N)
Herbivory treatments (H)
M0 6 20% Terrestrial habitat M1 = 40–45% Semi-aquatic habitat M2 = 100% Aquatic habitat
N0 = 0 g N m 2 Unfertilized N1 = 20 g N m 2 Fertilized
H0 = Control H1 = 10% leaf H2 = 20% leaf H3 = 50% leaf H4 = 90% leaf
removal removal removal removal
Herbivory was simulated by use of a steel hole punch. At the start of the study, 20 A. philoxeroides plants from five different locations in Wuhan were collected to measure the holes produced by herbivores, most of which were made by the introduced A. hygrophila and a native tortoise beetle, Cassida piperata Hope (Coleoptera: Chrysomelidae), on 10 leaves from each plant. The feeding holes were 2–7 mm in diameter for each beetle, which supports the use of a 6-mm diameter punch to simulate herbivory. The punch removed a portion of the leaf while leaving the mid-vein intact (Schooler et al., 2006). Leaf herbivory was simulated three times (31 August, 24 September, and 15 October) during the experiment to mimic repeated herbivore pressure. Plants assigned to simulated herbivory treatments were initially subjected to 10% leaf removal (H1), 20% leaf removal (H2), 50% leaf removal (H3), or 90% leaf removal (H4) (Table 1). The numbers of hole punches on each leaf were determined by the leaf area size. Using the Gravimetric method (Wu et al., 2007), three soil moisture levels were simulated: 620% (terrestrial, M0), 40–45% (semiaquatic, M1), and 100% (aquatic, M2) (Table 1). These values represent the different habitats where A. philoxeroides occurs. Soil moisture content was monitored and the pots were watered as necessary. From each pot, 6–15 g of soil was weighed before and after drying in an oven for 24 h at 104 °C. Plants assigned to fertilization treatments received either 0 g N m 2 (N0) or 20 g N m 2 (N1) during week two (starting 13 September) (Table 1). Slow release fertilizer (N:P:K = 15:15:15) was added as ammonium nitrate powder. 2.2. Data collection and statistical analysis
2. Materials and methods 2.1. Experimental design The experiment was conducted in a greenhouse at the Wuhan Botanical Institute/Wuhan Botanical Garden from July to October 2007. Average temperatures in the greenhouse were between 30–35 °C from July to September and 15–25 °C during October. Hundreds of A. philoxeroides plants were propagated from stems collected at Yuemachang, Wuhan on 31 July 2007. Stem cuttings (3000) that were 4–5 cm in length and each with one node were planted vertically in 43 32 11 cm plastic boxes. When the new shoots reached a height of approximately 5 cm (about 27 days after planting), the seedlings were repotted. Over 90% of the cuttings survived and the smallest 10% of plants were discarded. A total of 2400 plants were transplanted into 150 plastic containers (43 32 11 cm) on 1 September 2007. Each container had 16 plants, with each plant placed approximately 10 cm from its neighbors. Treatments were randomly assigned to each box in a full-factorial experimental design with five levels of simulated herbivory, two levels of fertilized addition, and three levels of soil moisture content (Table 1). Each treatment was replicated 20 times.
Random subsets of 20 plants per treatment combination (n = 600) were destructively sampled on three occasions: 15 September 2007 (day 15), 30 September 2007 (day 30), and 30 October 2007 (day 60). At each occasion the mass of roots, stems, and leaves, and the lengths of roots and stems were measured. From these measurements, total biomass and the ratio of root: shoot mass were calculated. Three-factor analysis of variance (ANOVA) was performed to analyze the effects of the range of environmental resource conditions (soil moisture, fertilization, and herbivory) on the biomass, root mass, stem mass, ratio of root: shoot mass, and growth rate of root length and of stem height. All data were analyzed using SPSS 13.0 for windows (SPSS Inc.) 3. Results 3.1. Total biomass Alternanthera philoxeroides total biomass was significantly affected by simulated herbivory and fertilization (Table 2). Increasing levels of simulated herbivory generally caused decreases in total biomass at all soil moisture levels (Fig. 1). At the first stage
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Table 2 Three-way analysis of variance tables comparing total biomass and root:shoot mass ratio for A. philoxeroides. The experimental treatments: H, simulated herbivory; N, fertilizer addition; M, soil moisture content at three sampling periods. Source
df
Total biomass
Root:shoot mass
Day 15
H N M HN HM NM HNM
4 1 2 4 8 2 8
Day 30
Day 60
Day 15
Day 30
Day 60
F
P
F
P
F
P
F
P
F
P
F
P
197.154 380.682 84.188 15.644 6.890 3.858 9.094
****
114.114 129.423 8.586 6.570 8.402 9.987 0.927
****
76.680 243.937 2.313 16.457 3.058 3.112 3.050
****
9.381 0.005 27.547 1.812 9.594 2.494 0.0694
****
46.230 11.232 5.951 0.849 2.189 0.390 1.379
****
28.150 0.348 79.041 1.309 24.196 11.740 0.905
****
**** **** **** **** * ****
**** **** **** **** ****
0.496
****
0.104 **** ** * **
0.944 ****
0.130 ****
0.086 0.696
*** **
0.496 *
0.677 0.210
0.556 ****
0.271 **** ****
0.515
*
P 6 0.05. P 6 0.01. P 6 0.001. **** P 6 0.0001. **
***
of this experiment (day 15, Fig. 1A), the difference in biomass between herbivory treatments (H0–H4) in the unfertilized group was smaller than that in the fertilized group, indicating a higher compensation capacity in unfertilized plants in a terrestrial habitat. However, there were no such differences between the two fertilized treatments in semi-aquatic and aquatic habitats. The biomass of the middle level of herbivory treatments (H3) at the
end of the experiment (day 60, Fig. 1C) was smallest in all of the three habitats. 3.2. Root:shoot (R/S) biomass ratio Alternanthera philoxeroides R/S ratio was significantly affected by simulated herbivory and soil moisture (Table 2). When plants
Fig. 1. Mean total biomass (g) for A. philoxeroides at three sampling dates (A: day 15, B: day 30, C: day 60) in full-factorial combination of five levels of simulated herbivory (H), two levels of fertilizer addition (N), and three levels of soil moisture content (M) treatments.
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suffered the highest level of simulated herbivory (H4), their R/S ratio in semi-aquatic and aquatic habitats increased significantly in the short term (Fig. 2B) but then decreased at the end of the experiment (Fig. 2C); however, the R/S ratio in the terrestrial habitat was maintained at a high level during the entire experiment (Fig. 2). At the end of the experiment (day 60), the R/S ratio of terrestrial habitat plants was significantly higher than semi-aquatic and aquatic habitats plants in the highest level of simulated herbivory treatment (H4), whereas the total biomass was not influenced when they grew in the same habitat, indicating more biomass was allocated to the below-ground portion of the plant in the terrestrial habitat. The R/S ratio increased more rapidly in the terrestrial habitat (M0) but very slowly in the aquatic habitat (M2) (Fig. 3 and Table 2). There was no significant effect of fertilizer on R/S ratio during the first or third sampling periods. However, fertilizer treatments significantly influenced R/S ratio during the second sampling period (Table 2).
Fig. 3. Mean root:shoot mass ratio for A. philoxeroides at three levels of soil moisture content (M) treatments during the experiment.
3.3. Growth rate Soil moisture treatments influenced root growth significantly. The root growth was slower in the aquatic habitat than in the terrestrial habitat. Herbivory and fertilizer treatments had no effect
on root growth (Table 3). The average root length growth rate per day (RLGR) (in 60 days) was higher in the terrestrial habitat than in the aquatic and semi-aquatic habitats (Fig. 4A). There was a significant interaction between herbivory and soil moisture on root
Fig. 2. Mean root:shoot mass ratio for A. philoxeroides at three sampling dates (A: day 15, B: day 30, C: day 60) in full-factorial combination of five levels of simulated herbivory (H), two levels of fertilizer addition (N), and three levels of soil moisture content (M) treatments.
Y. Sun et al. / Biological Control 48 (2009) 287–293 Table 3 Three-way analysis of variance tables comparing average root length growth rate and stem height growth rate for A. philoxeroides. The experimental treatments: H, simulated herbivory; N, fertilizer addition; M, soil moisture content during the entire experiment (60 days). Source
H N M HN HM NM HNM * **
df
4 1 2 4 8 2 8
Root length growth rate
Stem height growth rate
F
P
F
P
2.210 1.385 18.151 0.684 2.580 1.672 1.283
0.072 0.242
1.469 5.734 70.011 3.872 2.986 2.411 2.710
0.235
****
0.605 *
0.192 0.259
**** **** ****
0.055 0.053 **
P 6 0.05. P 6 0.01. P 6 0.0001.
****
growth in the terrestrial habitat (Table 3): the RLGR was lower in the second level herbivory treatment (H2) but increased significantly in the highest level herbivory treatment, when fertilized. Soil moisture and fertilization significantly influenced stem growth (Table 3 and Fig. 4B). The averaged stem height growth rate (STGR) was significantly higher in the aquatic habitat than in the terrestrial habitat. Fertilization significantly increased the stem growth in all the three habitats. There were no differences between the simulated herbivory level treatments; however, the interaction of simulated herbivory levels and fertilization significantly affected the STGR (Table 3). Plants that suffered the highest simulated herbivory level showed lower STGR when unfertilized, but when fertilized, their stems grew more rapidly. 4. Discussion By repeated destructive samplings, this study tested how a herbaceous plant recovered after simulated herbivory under different
291
environmental conditions. The results highlighted several important aspects which had not been addressed in previous studies. Here, we present two major findings: (i) A. philoxeroides had a higher tolerance to herbivory in terrestrial than in semi-aquatic and aquatic habitats, as indicated by higher root compensation in terrestrial habitats after simulated herbivory; (ii) the plant had higher tolerance under poor resource conditions, i.e., compensation capacity in the unfertilized treatment was higher than in the fertilized treatment. Simulated herbivory caused a decline in total biomass in all habitats. However, in general, A. philoxeroides appeared to respond differently to high levels of herbivory in the three habitats, with terrestrial plants showing the highest R/S biomass ratio. This indicates that the plant compensation capacity in terrestrial habitat is higher than that in other two habitats. The weed usually experiences more disturbance (e.g., natural enemies, fire, human-activities, etc.), in terrestrial habitats than aquatic habitats (Ma et al., 2003). Phenotypic adaptation may, therefore, explain the different compensation capacity between terrestrial and aquatic forms of A. philoxeroides. Moreover, above ground damage of terrestrial A. philoxeroides would create a nutrient sink which would drain nutrients from other parts of the plant, primarily from root tissues (Schooler et al., 2007). Interestingly, at the end of the experiment the plant’s total biomass and RLGR of the medium level herbivory treatments (H3) were the smallest in all the three habitats. This indicates that the compensation of A. philoxeroides may be influenced by damage level. When plants were damaged at the medium level (H3), the compensatory regrowth was lowest. Some unexpected trends were observed at day 30. Herbivory affected R/S ratio significantly in the aquatic and semi-aquatic habitats. Responses to herbivory may depend on the intrinsic growth rate of the plant species (Houle and Simard, 1996), the timing, type, and extent of herbivory (McNaughton, 1983; Rosenthal and Kotanen, 1994) and morphological or physiological traits that allow the plant to replace lost biomass (Tiffin, 2000). The particular
Fig. 4. Mean root length growth rate mass (A) and stem height growth rate mass (B) for A. philoxeroides at day 60 in full-factorial combination of three with five levels of simulated herbivory (H), two levels of fertilizer addition (N), and three levels of soil moisture content (M) treatments.
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time in the life cycle at which herbivory takes place may also play an important role (Prins et al., 1989). Therefore, these exceptions could have occurred because the second sampling period was only 5 days after simulated herbivory. In the case of R/S ratio, all plant roots were stimulated to grow quickly, but only the terrestrial A. philoxeroides could maintain a high R/S ratio at the highest level of simulated herbivory over the duration of the experiment. These findings indicate that A. philoxeroides demonstrates compensatory root growth after severe leaf herbivory, but that this response is more persistent in terrestrial than aquatic or semi-aquatic populations. For the second hypothesis, that A. philoxeroides would demonstrate greater tolerance in the nutrient-poor soil, we found that herbivory induced greater tolerance in unfertilized treatments than fertilized treatments in the terrestrial habitat at the first stage of the experiment (day 15), but fertilizer appeared not to influence tolerance at the middle and last stages of the experiment. Fertilizer was applied only once and may have been depleted over time. Future studies should use a gradient of fertilizer, applied at regular intervals throughout the experiment. Fertilizer affected SHGR significantly but had no effect on RLGR (Fig. 4A), implying different resource allocation strategies between above- and below-ground biomass, with different nutritional status. When the soil is nutrient poor, the damaged plant may allocate more nutrients to root growth to adapt to stressful environments, but allocates more resources to grow stems under favorable (nutrient-rich) conditions. Therefore, the results support the predictions of GRM: the weed is more tolerant in nutrient-poor soils. The results indicate a higher tolerance to herbivory by A. philoxeroides in terrestrial habitats than in aquatic habitats. Although it is known that the flea beetle, A. hygrophila is unable to control A. philoxeroides in terrestrial habitats due to low pupal survival on the solid-narrow hollow stems (Ma et al., 2003), the results may provide a supplementary explanation for the failure. The flea beetle has been considered an aquatic insect (Julien et al., 1995), however, its populations have been recently found on terrestrial forms of A. philoxeroides in Hubei Province, China (J. Ding, unpublished data). This study also indicates that biological control using leaf feeders would be more efficient in nutrient-rich conditions, as A. philoxeroides showed increased tolerance in nutrient-poor conditions than in nutrient-rich conditions. Therefore, the compensatory response of A. philoxeroides to other insect defoliators such as the alligator weed thrips, Amynothrips andersoni O’Neill (Thysanaptera: Phlaeothripidae) under different environmental conditions should be carefully considered in biological control programs. Local adaptability and phenotypic plasticity allow many exotic plant species to be highly invasive in variable environmental conditions (Ghalambor et al., 2007; Richards et al., 2006). Given the low success rate of classical biological control, i.e., only 33% released agents have successfully controlled target weeds (McFadyen, 1998), identifying the abiotic factors that affect the insect natural enemy’s ability to suppress the plant invader is critical to improve control efficacy. This study suggests that resource availability (water, nutrients, etc.) that often influences the growth and reproduction of invasive plant species may play an important role in biological control through regulating the plant tolerance to herbivory. Understanding mechanisms in plant invader compensation under different environmental conditions is important for improving management efficiency. Acknowledgments We thank Hongjun Dai, Yi Wang, Wenfeng Guo, Xinmin Lu, Wei Huang, Yangzhou Wang, Kai Wu, and Jialiang Zhang for their field and lab assistance. The comments of Michael J. Wise, Heinz Müller-Schärer, Ashley K. Baldridge, Matthew A. Barnes, John
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