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Yongge Yuan, Huifei Jin, Junmin Li, Effects of latitude and soil microbes on the resistance of invasive Solidago canadensis to its co-evolved insect herbivore Corythucha marmorata, Journal of Plant Ecology, Volume 15, Issue 3, June 2022, Pages 549–560, https://doi.org/10.1093/jpe/rtab093
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Abstract
There is an increasing likelihood that invasive plants are again exposed to their co-evolved specialist herbivores in the non-native range. However, whether there is a latitudinal pattern associated with the resistance of an invasive plant to its co-evolved herbivores and how soil microbes affect resistance has been little explored. We hypothesized that the resistance of invasive Solidago canadensis to its co-evolved insect herbivore Corythucha marmorata could increase with latitude, and that local rhizosphere microbes could facilitate invasive plants to become resistant to their co-evolved herbivores. We conducted a field survey and a greenhouse experiment to examine whether there was a latitudinal pattern in the abundance of C. marmorata and in the damage it caused to S. canadensis in China. We tested whether local rhizosphere microbes of invasive plants can promote the resistance of S. canadensis to C. marmorata herbivory. In the field survey, both density of C. marmorata and damage level of S. canadensis were positively correlated with latitude, and with S. canadensis plant growth, indicating a latitudinal pattern in the resistance of S. canadensis to C. marmorata. However, in the greenhouse experiment, S. canadensis from different latitudes did not suffer significantly from different levels of damage from C. marmorata. Additionally, the damage level of S. canadensis was lower when rhizosphere soil and rhizomes originated from field S. canadensis with same damage level than with different damage levels. This result indicates that local rhizosphere soil microbes promote the adaptation of S. canadensis to resistance of C. marmorata.
摘要
在全球化的背景下,入侵植物再次暴露在来自其原产地的专性食草动物面前的可能性越来越大。然而,入侵植物对曾共同进化的专性食草动物的抗性是否存在纬度趋势以及土壤微生物如何影响入侵植物对这类食草动物的抗性还鲜有研究。我们假设入侵植物加拿大一枝黄花(Solidago canadensis)对其曾共 同进化的来自原产地的食草昆虫菊方翅网蝽(Corythucha marmorata)的抗性随纬度的增加而增加,而加拿 大一枝黄花的局部根际微生物可以促进加其对菊方翅网蝽的抗性。为了验证上述假设,我们首先通过野外调查和温室实验,研究了菊方翅网蝽在中国加拿大一枝黄花种群中的分布丰度,以及对加拿大一枝黄花造成的危害是否存在纬度分布规律。其次,我们通过温室实验,检测了加拿大一枝黄花的本地根际土壤微生物是否能促进加拿大一枝黄花对菊方翅网蝽的抗性。研究结果表明,菊方翅网蝽在加拿大一枝黄花中的分布密度和对加拿大一枝黄花的危害程度与纬度以及加拿大一枝黄花的生长呈现正相关,说明加拿大一枝黄花对菊方翅网蝽的抗性具有纬度趋势。然而,在温室实验中,来自不同纬度的加拿大一枝黄花受到菊方翅网蝽的伤害程度没有显著差异。此外,当根际土壤和加拿大一枝黄花的根状茎同时来自于野外被轻度危害的加拿大一枝黄花或同时来自于野外被重度危害的加拿大一枝黄花时,加拿大一枝黄花的抗性最强。这一结果表明,加拿大一枝黄花的局部根际土壤微生物促进了加拿大一枝黄花对菊方翅网蝽的抗性。
INTRODUCTION
With the onset of economic globalization, numerous plant species have been introduced into new biogeographical areas over recent decades (Seebens et al. 2017; van Kleunen et al. 2015). Some of the introduced species have spread widely and are now dominant in their new ranges, thus altering ecological processes (Gioria and Osborne 2014; Vitousek et al. 1996). Various hypotheses, including the enemy release hypothesis, have been formulated to explain why certain plants become invasive in their introduced ranges (Blossey and Notzold 1995; Callaway and Aschehoug 2000; Li et al. 2020; Wan et al. 2019; Yang et al. 2021). The enemy release hypothesis posits that some plants become successful invaders because they escape specialist natural enemies (i.e. herbivores and pathogens) in their invasive ranges (Keane and Crawley 2002). However, some invasive plant species have been reunited with their co-evolved herbivores either through intentional introduction in biological control programmes or through accidental introductions (Wan et al. 2019; Zangerl et al. 2005). Exploring the interactions between invasive plants and their co-evolved herbivores in non-native ranges can help to evaluate how such reunions affect ecosystems.
Interactions between plants and herbivores may vary geographically and show latitudinal patterns (Pennings et al. 2009; Sotka and Hay 2002). The latitudinal biotic interaction hypothesis posits that as latitude decreases, interactions between plants and herbivores are strengthened (Schemske et al. 2009). Several studies have shown that herbivores were more abundant and caused greater damage to them at low-latitude sites relative to high-latitude sites (Pennings et al. 2009; Pennings and Silliman 2005). Moreover, studies have shown that such a latitudinal pattern also exists in the interactions between invasive plants and herbivores (Cronin et al. 2015; Lu et al. 2019). For example, Lu et al. (2019) found that herbivore abundance decreased with latitude and appeared to promote the invasion of Alternanthera philoxeroides at low but not high latitudes. However, how the defence of invasive plants against their re-associated co-evolved herbivores changes with latitude in their invaded range remains scarcely explored.
Local adaptation is described as a pattern of divergent selection among local environments that drives populations to evolve divergently under specific ecological conditions (Macel et al. 2007; Williams 1966). Local adaptation should be manifested in improved fitness of each deme in its own habitat in a reciprocal transplant or common garden ‘explant’ experiment (Kawecki and Ebert 2004). Studies have shown that local adaptation in plants can be driven by closely associated microbes (Kalske et al. 2012; Rodriguez and Redman 2008). For example, salt-tolerant Hibiscus hamabo performed better with rhizosphere microbes from the same site compared with treatments with foreign rhizosphere microbes (Yuan et al. 2019). However, whether local rhizosphere soil biota of invasive plant promotes the defence of invaders against their co-evolved herbivores remains unclear.
The re-association between the invasive plant, Solidago canadensis (Asteraceae), and the lace bug, Corythucha marmorata (Tingidae: Hemiptera), provides an ideal system for understanding the interaction between invasive plants and their co-evolved herbivores from their native range. Solidago canadensis, a plant species native to North America, was first introduced to China as an ornamental plant in the 1910s and then rapidly spread along the southeast coast of China (Dong et al. 2006; Weber 1997). It has become one of the most serious invasive weeds in China (Sun et al. 2006). Solidago canadensis can propagate via both seeds and rhizomes (Zhang et al. 2009). Corythucha marmorata, an important natural enemy of S. canadensis in its native range North American, was first found in Shanghai, China in 2010 (Dang et al. 2012). It has subsequently spread to surrounding regions, including Zhejiang, Jiangxi, and Jiangsu provinces (Cai et al. 2019; Lu et al. 2018; Shen et al. 2016). The main host of C. marmorata are Asteraceae plants, such as S. canadensis and Ambrosia artemisiifolia (Watanabe and Shimizu 2015, 2017). The average length of immature stages of C. marmorata was 15 days, the adult average life span was 60 days, and the number of progeny per female was 87 (Shen et al. 2016). Corythucha marmorata herbivory is distinguished from herbivory by other insect species by its distinctive yellow feeding scars (Sakata et al. 2017) resulting from the species piercing the epidermis and sucking the contents of mesophyll cells (Maddox and Root 1990). At present, Corythucha marmorata is still expanding its distribution within China.
In our study, we conducted a field survey and a greenhouse experiment to examine whether there was a latitudinal pattern in the resistance of S. canadensis to C. marmorata in China. Moreover, we performed a greenhouse experiment to test whether the local rhizosphere microbes of invasive plants could help S. canadensis to resist C. marmorata herbivory. We had the following hypotheses: (i) the resistance of invasive S. canadensis to C. marmorata increases with latitude and (ii) local rhizosphere microbes facilitate the resistance of S. canadensis to C. marmorata.
MATERIALS AND METHODS
Field survey
To estimate whether there was a latitudinal pattern of the resistance of the invasive plant S. canadensis to C. marmorata, its co-evolved herbivore, in the field, we conducted a survey in six cities ranging from 28° N to 31.1° N in terrestrial habitats in southeast China from July to August 2019 (Fig. 1; Supplementary Table S1). Most surveyed sites were located in roadsides and waste lands (Supplementary Table S1). Three sites were surveyed in each city, with the exception of Wenzhou, where only two sites were surveyed. In each city, the distance between any two adjacent sites was at least 2 km, and the patch size of S. canadensis in each site was >50 m2. We randomly chose three 2 m × 2 m quadrats (>5 m apart) at each site. Six S. canadensis individuals from different genets in each quadrat were surveyed. Genets of S. canadensis can easily be recognized in the field based on the formation of dense clusters of stems (Li et al. 2016). For each S. canadensis plant individual, the density of C. marmorata and damage level of plant growth traits, including the number of leaves, height, and stem length, were recorded. In addition, we calculated the damage level to estimate the damage from C. marmorata. First, the level of C. marmorata herbivory in each S. canadensis individual was also assessed by classifying the leaves damaged by C. marmorata into one of four levels based on the percentage of damaged total leaf area: (i) no damage, (ii) <33% damage, (iii) 33%–66% damage and (iv) >66% damage. Then, we counted the number of leaves at each damage level. The damage level was calculated by summing the values across all four levels and dividing this figure by the total leaf number (Sakata et al. 2017). Additionally, the leaves of each surveyed S. canadensis individual were collected and brought back to the laboratory to be dried at 65 °C until they reached a constant weight. The rhizomes and rhizosphere soil samples of each surveyed S. canadensis plant were also collected for further greenhouse experiments (Experiment 1 and Experiment 2). To reduce the chance of sampling the same genet more than once, all collected rhizomes were separated from each other by at least 10 m (Li et al. 2016). Rhizomes were brought back to the laboratory and transplanted separately into pots in the greenhouse for one growing season to reduce environmental carry-over effects (Li et al. 2016). All pots were randomly arranged in a greenhouse with a 16 h/8 h light/dark photoperiod, with an 18 °C/25 °C (night/day) temperature regime. The rhizosphere soil was stored in a refrigerator at −20 °C.
A simple linear regression model (y = a + bx) was used to fit a straight line to the relationship between latitude and the density of C. marmorata on each S. canadensis plant, the damage level, and growth traits of S. canadensis (i.e. leaf biomass, height, number of leaves, stem length). Spearman correlation analysis was performed to determine the relationships between the density of C. marmorata or damage level of plant growth traits (i.e., leaf biomass, height, number of leaves, stem length). When a significant correlation was found, a simple linear regression model (y = a + bx) was fitted. SPSS (V.16.0, SPSS Inc., Chicago, IL, USA) was used for all statistical analyses in this study.
Experiment 1
This experiment was designed to estimate whether latitudinal pattern of the resistance of the invasive plant S. canadensis to C. marmorata was present in greenhouse. In June 2020, we randomly chose newly produced ramets with a height of about 15 cm from 12 stock genotypes of S. canadensis sampled from different latitudes. The rhizome segments were washed with tap water, soaked in 10% NaClO for 15 min and washed with tap water again. Then, the segments were individually planted in pots filled with substrate, yielding a total of 72 (6 latitudes × 12 replicates) pots. After a 2-month growth period in a greenhouse, each S. canadensis individual was covered with a nylon bag (20 cm × 30 cm). Then, half of the pots corresponding to each latitude were each inoculated with 40 adult C. marmorata, which were collected from the Taizhou University campus, while the other half of the pots (without any inoculation) were treated as the control. One month after the inoculation, we measured the number of leaves and the damage level caused by S. canadensis. The damage level of S. canadensis was calculated using the method described in the field survey portion of this study. Then, we harvested all S. canadensis plants, and their leaves, stems, and roots were harvested separately and oven dried at 65 °C to a constant weight.
A simple linear regression model (y = a + bx) was used to fit a straight line to the relationships between latitude and shoot biomass, leaf biomass and the number of leaves under the control and herbivory treatments. To determine whether the slopes of the regression lines significantly differed between control and herbivory treatments, the homogeneity of the slopes (i.e. parallelism) was tested via one-way ANCOVA. Regression lines describing the relationships between latitude and shoot biomass, leaf biomass and number of leaves that were significantly nonparallel indicated that the effect of latitude on shoot biomass, leaf biomass and number of leaves were significantly different between control and herbivory treatments.
Additionally, a Spearman correlation analysis was performed to assess the relationship between damage level and latitude. When a significant correlation was found, a simple linear regression model (y = a + bx) was fitted. The effects of herbivory and latitude on the growth of S. canadensis were tested using two-way analysis of variance (ANOVA). The effects of latitude on the damage level of S. canadensis were tested using one-way ANOVAs. Mean values were compared using least significant difference (LSD) tests at a P < 0.05 significance level.
Experiment 2
A two-factor full factorial experiment was designed to test whether and how rhizosphere soil microbes affect the resistance of S. canadensis to C. marmorata. In October 2019, we chose 12 ramets from 12 rhizome samples of S. canadensis with a high damage level in the field along with 12 corresponding rhizosphere soil samples. Additionally, another 12 ramets from 12 rhizome samples of S. canadensis with a low damage level were selected, along with 12 corresponding rhizosphere soil samples. Each selected ramet and each rhizosphere soil sample were from a S. canadensis collection site with different genotypes. The experiment included three factors: (i) two ramet origins, (ii) two rhizosphere soil origins (low versus high damage or local versus foreign) and (iii) herbivory or no herbivory. The substrate used here was sterilized by autoclaving for 2 h at 121 °C. Then, the sterilized substrate was inoculated with the 24 rhizosphere soil samples. The inocula (rhizosphere soil) and substrate were mixed at a ratio of 1:20 (v/v) (Lau and Lennon 2012). Ramets of similar length were washed with tap water, soaked in 10% NaClO for 15 min and then washed with tap water again. Then, each of 24 ramets were planted in a pot filled with substrate and inoculum, yielding a total of 24 (two ramet origins × two rhizosphere soil origins × two herbivory treatments × three replicates) pots with following treatments: (i) six high damage ramets with six local high damage rhizosphere soil samples, (ii) six high damage ramets with six foreign low damage rhizosphere soil samples, (iii) six low damage ramets with six local low damaged rhizosphere soil samples and (iv) six low damage ramets with six foreign high damage rhizosphere soil samples. All pots were randomly arranged in the same greenhouse used for Experiment 1. After a 2-month growth period, half of the pots for each treatment were treated with C. marmorata using the same methods as used in Experiment 1. The other half of the pots that had not been inoculated were treated as the control. One month after the inoculation, we measured the damage level of S. canadensis. First, the damage level of S. canadensis was calculated using the method described in the field survey. Then, we harvested all S. canadensis plants, and the leaves, stems and roots were harvested separately and oven dried at 65 °C to a constant weight.
The effects of plant origin, rhizosphere soil origin (low versus high damage) and herbivory on the response of S. canadensis to C. marmorata were tested using three-way ANOVA after variance homogeneity was confirmed. The effects of plant origin and rhizosphere soil origin (low versus high damage) on the damage level of S. canadensis and the survival rate of C. marmorata were tested using two-way ANOVA after variance homogeneity was confirmed as well. In addition, to test whether the rhizosphere soil promoted resistance of S. canadensis to C. marmorata when the damage level of rhizosphere soil and rhizomes matched, we also conducted an ANOVA using a source factor, i.e. local versus foreign. The local-foreign test is frequently used in studies on local adaptation (Kawecki and Ebert 2004; Yuan et al. 2019). A lower damage level of S. canadensis originated from the local population (high/low damage plants with rhizosphere soil from high/low damage plants) than from the foreign populations (high/low damage plants with rhizosphere soil from low/high damage plants) would indicate local adaptation (Kawecki and Ebert 2004; Yuan et al. 2019). Then, treatment mean values were compared by using the LSD test at a P < 0.05 significance level.
RESULTS
Field survey
Leaf biomass, number of leaves and stem length of S. canadensis, which were well-established proxies for fitness, were not significantly related with latitude (P > 0.05, Fig. 2a–c). The height of S. canadensis was significantly negatively related with latitude (P < 0.05, Fig. 2d). The density of C. marmorata in each plant and damage level of S. canadensis was significantly positively related with latitude (P < 0.05, Fig. 2e and f). The density of C. marmorata was significantly associated with the damage level of S. canadensis (Supplementary Fig. S1).
The density of C. marmorata was significantly associated with leaf biomass, number of leaves and stem length of S. canadensis (P < 0.05, Supplementary Fig. S2a–c), but was not significantly associated with the height of S. canadensis (P > 0.05, Supplementary Fig. S2d).
The damage level of S. canadensis was significantly associated with the leaf biomass and stem length of S. canadensis (P < 0.05, Supplementary Fig. S3a and c), but was not significantly associated with the number of leaves or height of S. canadensis (P > 0.05, Supplementary Fig. S3b and d).
Experiment 1
The shoot biomass, leaf biomass and number of leaves of S. canadensis were not significantly related with latitude under either the control or herbivory treatments (P > 0.05, Fig. 3a–c). The effects of latitude on shoot biomass, leaf biomass and number of leaves were not significantly different between the control and herbivory treatment (P > 0.05, Fig. 3a–c). The damage level of S. canadensis was not significantly associated with latitude (P > 0.05, Fig. 3d).
LSD tests showed that herbivory did not significantly reduce shoot biomass, root biomass or height of S. canadensis within each latitude (Supplementary Fig. S4a, c and d). However, herbivory significantly increased leaf biomass of S. canadensis when rhizomes of S. canadensis originated from Shanghai (Supplementary Fig. S4b).
Experiment 2
Statistical analysis revealed that plant origin, soil origin (low versus high damage) and herbivory treatment did not significantly affect shoot biomass, leaf biomass, root biomass, damage level of S. canadensis or the survival rate of C. marmorata. Additionally, there were no significant interactive effects among plant origin, soil origin and herbivory treatments on biomass of shoot, leaf and root tissues. However, there was a significant interactive effect between plant origin and soil origin treatment on S. canadensis damage level (P = 0.042, Table 1). The LDS tests showed that there were no significant differences in shoot biomass, leaf biomass and total biomass of S. canadensis or in survival rate of C. marmorata among the different treatments (Fig. 4a–c; Supplementary Fig. S6); however, the damage level of S. canadensis was significantly lower when both rhizosphere soil and rhizomes originated from S. canadensis field sites with the same damage level than from S. canadensis field sites with different damage levels (Supplementary Table S2; Fig. 4d; Supplementary Fig. S5).
. | Factors . | df . | F . | P . |
---|---|---|---|---|
Shoot biomass | Plant origin (PO) | 1 | 0.388 | 0.542 |
Soil origin (SO) | 1 | 0.326 | 0.576 | |
Herbivory (H) | 1 | 1.996 | 0.177 | |
PO × SO | 1 | 0.292 | 0.597 | |
PO × H | 1 | 0.004 | 0.949 | |
SO × H | 1 | 0.589 | 0.454 | |
PO × SO × H | 1 | 0.817 | 0.379 | |
Leaf biomass | Plant origin (PO) | 1 | 1.310 | 0.269 |
Soil origin (SO) | 1 | 0.388 | 0.542 | |
Herbivory (H) | 1 | 1.3178 | 0.268 | |
PO × SO | 1 | 0.127 | 0.726 | |
PO × H | 1 | <0.001 | 0.985 | |
SO × H | 1 | 0.073 | 0.791 | |
PO × SO × H | 1 | 0.099 | 0.757 | |
Total biomass | Plant origin (PO) | 1 | 0.594 | 0.452 |
Soil origin (SO) | 1 | 0.303 | 0.589 | |
Herbivory (H) | 1 | 2.414 | 0.140 | |
PO × SO | 1 | 0.0612 | 0.807 | |
PO × H | 1 | 0.002 | 0.968 | |
SO × H | 1 | 0.910 | 0.354 | |
PO × SO × H | 1 | 1.171 | 0.295 | |
Damage level | Plant origin (PO) | 1 | 0.138 | 0.720 |
Soil origin (SO) | 1 | 0.028 | 0.871 | |
PO × SO | 1 | 5.875 | 0.042* | |
Survival rate | Plant origin (PO) | 1 | 0.225 | 0.648 |
Soil origin (SO) | 1 | 0.225 | 0.648 | |
PO × SO | 1 | 3.025 | 0.120 |
. | Factors . | df . | F . | P . |
---|---|---|---|---|
Shoot biomass | Plant origin (PO) | 1 | 0.388 | 0.542 |
Soil origin (SO) | 1 | 0.326 | 0.576 | |
Herbivory (H) | 1 | 1.996 | 0.177 | |
PO × SO | 1 | 0.292 | 0.597 | |
PO × H | 1 | 0.004 | 0.949 | |
SO × H | 1 | 0.589 | 0.454 | |
PO × SO × H | 1 | 0.817 | 0.379 | |
Leaf biomass | Plant origin (PO) | 1 | 1.310 | 0.269 |
Soil origin (SO) | 1 | 0.388 | 0.542 | |
Herbivory (H) | 1 | 1.3178 | 0.268 | |
PO × SO | 1 | 0.127 | 0.726 | |
PO × H | 1 | <0.001 | 0.985 | |
SO × H | 1 | 0.073 | 0.791 | |
PO × SO × H | 1 | 0.099 | 0.757 | |
Total biomass | Plant origin (PO) | 1 | 0.594 | 0.452 |
Soil origin (SO) | 1 | 0.303 | 0.589 | |
Herbivory (H) | 1 | 2.414 | 0.140 | |
PO × SO | 1 | 0.0612 | 0.807 | |
PO × H | 1 | 0.002 | 0.968 | |
SO × H | 1 | 0.910 | 0.354 | |
PO × SO × H | 1 | 1.171 | 0.295 | |
Damage level | Plant origin (PO) | 1 | 0.138 | 0.720 |
Soil origin (SO) | 1 | 0.028 | 0.871 | |
PO × SO | 1 | 5.875 | 0.042* | |
Survival rate | Plant origin (PO) | 1 | 0.225 | 0.648 |
Soil origin (SO) | 1 | 0.225 | 0.648 | |
PO × SO | 1 | 3.025 | 0.120 |
* indicate the level of statistical significance (P < 0.05).
. | Factors . | df . | F . | P . |
---|---|---|---|---|
Shoot biomass | Plant origin (PO) | 1 | 0.388 | 0.542 |
Soil origin (SO) | 1 | 0.326 | 0.576 | |
Herbivory (H) | 1 | 1.996 | 0.177 | |
PO × SO | 1 | 0.292 | 0.597 | |
PO × H | 1 | 0.004 | 0.949 | |
SO × H | 1 | 0.589 | 0.454 | |
PO × SO × H | 1 | 0.817 | 0.379 | |
Leaf biomass | Plant origin (PO) | 1 | 1.310 | 0.269 |
Soil origin (SO) | 1 | 0.388 | 0.542 | |
Herbivory (H) | 1 | 1.3178 | 0.268 | |
PO × SO | 1 | 0.127 | 0.726 | |
PO × H | 1 | <0.001 | 0.985 | |
SO × H | 1 | 0.073 | 0.791 | |
PO × SO × H | 1 | 0.099 | 0.757 | |
Total biomass | Plant origin (PO) | 1 | 0.594 | 0.452 |
Soil origin (SO) | 1 | 0.303 | 0.589 | |
Herbivory (H) | 1 | 2.414 | 0.140 | |
PO × SO | 1 | 0.0612 | 0.807 | |
PO × H | 1 | 0.002 | 0.968 | |
SO × H | 1 | 0.910 | 0.354 | |
PO × SO × H | 1 | 1.171 | 0.295 | |
Damage level | Plant origin (PO) | 1 | 0.138 | 0.720 |
Soil origin (SO) | 1 | 0.028 | 0.871 | |
PO × SO | 1 | 5.875 | 0.042* | |
Survival rate | Plant origin (PO) | 1 | 0.225 | 0.648 |
Soil origin (SO) | 1 | 0.225 | 0.648 | |
PO × SO | 1 | 3.025 | 0.120 |
. | Factors . | df . | F . | P . |
---|---|---|---|---|
Shoot biomass | Plant origin (PO) | 1 | 0.388 | 0.542 |
Soil origin (SO) | 1 | 0.326 | 0.576 | |
Herbivory (H) | 1 | 1.996 | 0.177 | |
PO × SO | 1 | 0.292 | 0.597 | |
PO × H | 1 | 0.004 | 0.949 | |
SO × H | 1 | 0.589 | 0.454 | |
PO × SO × H | 1 | 0.817 | 0.379 | |
Leaf biomass | Plant origin (PO) | 1 | 1.310 | 0.269 |
Soil origin (SO) | 1 | 0.388 | 0.542 | |
Herbivory (H) | 1 | 1.3178 | 0.268 | |
PO × SO | 1 | 0.127 | 0.726 | |
PO × H | 1 | <0.001 | 0.985 | |
SO × H | 1 | 0.073 | 0.791 | |
PO × SO × H | 1 | 0.099 | 0.757 | |
Total biomass | Plant origin (PO) | 1 | 0.594 | 0.452 |
Soil origin (SO) | 1 | 0.303 | 0.589 | |
Herbivory (H) | 1 | 2.414 | 0.140 | |
PO × SO | 1 | 0.0612 | 0.807 | |
PO × H | 1 | 0.002 | 0.968 | |
SO × H | 1 | 0.910 | 0.354 | |
PO × SO × H | 1 | 1.171 | 0.295 | |
Damage level | Plant origin (PO) | 1 | 0.138 | 0.720 |
Soil origin (SO) | 1 | 0.028 | 0.871 | |
PO × SO | 1 | 5.875 | 0.042* | |
Survival rate | Plant origin (PO) | 1 | 0.225 | 0.648 |
Soil origin (SO) | 1 | 0.225 | 0.648 | |
PO × SO | 1 | 3.025 | 0.120 |
* indicate the level of statistical significance (P < 0.05).
DISCUSSION
According to the latitudinal biotic interaction hypothesis, a decrease in latitude should strengthen the interaction between plants and herbivores (Pennings et al. 2009; Pennings and Silliman 2005; Schemske et al. 2009). However, our study contrarily showed that C. marmorata, which is a S. canadensis herbivore occurring in its native range, was more abundant and caused greater damage to invasive S. canadensis at higher latitudes in the invaded region of China. As a co-evolved natural enemy of invasive S. canadensis in its native range in North America, the warm temperate zone at high altitudes is a suitable habitat for both species. Previous studies have also shown that temperature was the main factor affecting herbivory (Liu et al. 2022; Zhang et al. 2016) and the distribution of C. marmorata (Sakata et al. 2017; Wang et al. 2019). The temperature of the surveyed sites at higher latitudes in our study might be more suitable for the growth of C. marmorata. The adaptation of both invasive S. canadensis and its co-evolved enemy to climates at high altitudes in its native range might determine the vigorous growth of both and their adaption to the climate at high altitudes in its invaded range in China.
However, we found that the latitudinal pattern of C. marmorata density and damage C. marmorata caused to invasive S. canadensis was absent in the common garden greenhouse experiment. C. marmorata was first found in China in 2010 (Dang et al. 2012), and there has thus been a very short history of interactions between C. marmorata and invasive S. canadensis in China and insufficient time for C. marmorata to expand its range within China. A recent study has shown that latitudinal clines in traits related to herbivory can be shaped within 100 years (Bhattarai et al. 2017). There may not have been sufficient exposure time for S. canadensis to evolve resistance to C. marmorata within China (only 10 years). Besides, the field survey in our study was conducted across only three latitudes. The short history of expansion and the narrow latitudinal range might weaken the observed latitudinal pattern of the interaction between invasive S. canadensis and C. marmorata herbivory. To find empirical support for the latitudinal biotic interaction hypothesis in this system will require monitoring of the effect of C. marmorata on S. canadensis across a wider latitudinal scale.
Moreover, compensatory growth can be induced by herbivory. Notably, in this study, we did not find deterioration in the effect of herbivory on shoot biomass, root biomass or height of S. canadensis, indicating the loss of the effectiveness of C. marmorata as a control agent for S. canadensis in greenhouse conditions. Compensatory growth was also found in previous studies, which showed that moderate herbivory may have weak effects on invasive weeds and perhaps stimulate compensatory growth responses (Zong and Shi 2019). For example, in the greenhouse experiment conducted by Lu and Ding (2012), compensatory effects, inhibitory effects and absent effects were all detected in different Alternanthera philoxeroides populations treated with herbivory. In our study, the leaf biomass of S. canadensis originating from Shanghai increased under herbivory (Supplementary Fig. S4b). Thus, the compensatory growth of S. canadensis might offset the effect of herbivory on S. canadensis.
In this study, we also found that the origins of both rhizomes and rhizosphere soil samples did not significantly affect the growth and herbivory level of S. canadensis in the greenhouse. However, there was a significant interactive effect between the origin of rhizomes and the origin of rhizosphere soil on the damage level of S. canadensis (Table 1). This indicated that when rhizomes and rhizosphere soil samples originated from S. canadensis field sites with identical herbivory levels, resistance to C. marmorata of S. canadensis in the greenhouse was relatively higher (Fig. 4d). This result was consistent with our hypothesis that local rhizosphere microbes could facilitate invasive plants to become resistant to their co-evolved herbivores. Beneficial microbes belowground can improve plant health to increase their defence against insect herbivores (Pieterse et al. 2014). For example, Allsup and Paige (2016) found that belowground mycorrhizal fungi enhance the tolerance of Ipomopsis aggregata to herbivory. Our results indicated soil microbes play important roles in the resistance of S. canadensis populations in response to herbivores, irrespective of whether they come from populations with low or high resistance. That is, S. canadensis populations exposed to herbivores are associated with beneficial soil microbes that enhance the resistance of S. canadensis to herbivores. This might be owing to the induction of systemic resistance (ISR) against insect herbivores in plants as mediated by beneficial soil microbes (Harun-Or-Rashid and Chung 2017). ISR is activated by non-pathogenic bacteria in salicylic acid-independent and -dependent manners and somewhat involves the jasmonic acid/ethylene pathway (Harun-Or-Rashid and Chung 2017). Several types of rhizobacteria induce biochemical changes that trigger ISR in plants against insect herbivores (Wielkopolan and Obrepalska-Steplowska 2016; Zebelo et al. 2016). Therefore, when S. canadensis and C. marmorata became re-associated, the beneficial soil microbes produced and triggered ISR in S. canadensis against insect herbivores. However, the potential mechanism through which soil microbial communities from both low- and high-resistance S. canadensis populations could have enhanced the resistance of S. canadensis to newly re-associated C. marmorata in the present study remains unresolved. Future studies should test for ISR in roots of S. canadensis in response to C. marmorata mediated by beneficial soil microbes.
Although many previous studies have shown that the absence of pressure from native enemies promotes the invasion of exotic plants in non-native ranges (Beckmann et al. 2016; Dong et al. 2017; Fornoni 2011), few studies have explored whether and how invasive plants interact with their co-evolved enemies from their native ranges (Fukano and Yahara 2012; Sakata et al. 2017; Wan et al. 2019). The re-association between the invasive plant S. canadensis and C. marmorata provides an ideal system for understanding the interaction between invasive plants and co-evolved herbivores from their native range. Exploring the defence of S. canadensis to C. marmorata would help to evaluate the efficiency of biological control for S. canadensis and would also help to predict the possible ecological consequences of C. marmorata. Our results demonstrated that the resistance of S. canadensis to its co-evolved herbivore C. marmorata exhibited a latitudinal pattern in the field, but this pattern was not observed in common greenhouse conditions. Our results also showed that local soil biota associated with S. canadensis increased its resistance to C. marmorata. These results clarify the relationship between invasive S. canadensis and its co-evolved herbivore from its native range, thus informing the management of invasive S. canadensis.
Supplementary Material
Supplementary material is available at the Journal of Plant Ecology online.
Table S1: Field survey site summary.
Table S2: Effect of plant origins and soil origins (local versus foreign) on the damage level of S. canadensis in Experiment 2.
Figure S1: Relationship between damage level of Solidago canadensis and the density of Corythucha marmorata in the field survey. The linear regression curve is shown in the figure if the correlation is positive.
Figure S2: Relationship between the density of Corythucha marmorata on Solidago canadensis with leaf biomass (a), number of leaves (b), stem length (c), and height (d) of S. canadensis.
Figure S3: Relationship between the damage level and leaf biomass (a), number of leaves (b), stem length (c), and height (d) of Solidago canadensis.
Figure S4: Effects of cities with different latitudes and herbivory treatments on plant traits of Solidago canadensis, including shoot biomass (a), leaf biomass (b), root biomass (c), and height (d) in Experiment 1. SZ, SH, HZ, NB, TZ, and WZ indicate that the rhizomes originated from Suzhou, Shanghai, Hangzhou, Ningbo, Taizhou, and Wenzhou, respectively.
Figure S5: The effect of plant origin and soil origin (low versus high damage) on damage level of Solidago canadensis in Experiment 2.
Figure S6: The effect of plant origin and soil origin (low versus high damage) on survival rate of Corythucha marmorata in Experiment 2.
Funding
This work was supported by the Ten Thousand Talent Program of Zhejiang Province (2019R52043), the National Key Research and Development Program of China (2016YFC1201100) and the National Natural Science Foundation of China (31270461).
Conflict of interest statement. The authors declare that they have no conflict of interest.