Genomic and phenotypic signatures provide insights into the wide adaptation of a global plant invader.

Invasive alien species are primary drivers of biodiversity loss and species extinction. Smooth cordgrass (Spartina alterniflora) is one of the most aggressive invasive plants in coastal ecosystems around the world. However, the genomic bases and evolutionary mechanisms underlying its invasion success have remained largely unknown. Here, we assembled a chromosome-level reference genome and performed phenotypic and population genomic analyses between native US and introduced Chinese populations. Our phenotypic comparisons showed that introduced Chinese populations have evolved competitive traits, such as early flowering time and greater plant biomass, during secondary introductions along China's coast. Population genomic and transcriptomic inferences revealed distinct evolutionary trajectories of low- and high-latitude Chinese populations. In particular, genetic mixture among different source populations, together with independent natural selection acting on distinct target genes, may have resulted in high genome dynamics of the introduced Chinese populations. Our study provides novel phenotypic and genomic evidence showing how smooth cordgrass rapidly adapts to variable environmental conditions in its introduced ranges. Moreover, candidate genes related to flowering time, fast growth, and stress tolerance (i.e., salinity and submergence) provide valuable genetic resources for future improvement of cereal crops.

Restoration of native saltmarshes can reverse arthropod assemblages and trophic interactions changed by a plant invasion.

Plant invasions profoundly impact both natural and managed ecosystems, and removal of the invasive plants addresses only part of the problem of restoring impacted areas. The rehabilitation of diverse communities and their ecosystem functions following removal of invasive plants is an important goal of ecological restoration. Arthropod assemblages and trophic interactions are important indicators of the success of restoration, but they have largely been overlooked in saltmarshes. We determined how arthropod assemblages and trophic interactions changed with the invasion of the exotic plant Spartina alterniflora and with the restoration of the native plant Phragmites australis following Spartina removal in a Chinese saltmarsh. We investigated multiple biotic and abiotic variables to gain insight into the factors underlying the changes in arthropod assemblages and trophic structure. We found that although Spartina invasion had changed arthropod diversity, community structure, feeding-guild composition, and the diets of arthropod natural enemies in the saltmarsh, these changes could be reversed by the restoration of native Phragmites vegetation following removal of the invader. The variation in arthropod assemblages and trophic structure were critically associated with four biotic and abiotic variables (aboveground biomass, plant density, leaf N, and soil salinity). Our findings demonstrate the positive effects of controlling invasive plants on biodiversity and nutrient cycling and provide a foundation for assessing the efficacy of ecological restoration projects in saltmarshes.

Global synthesis of effects of plant species diversity on trophic groups and interactions.

Numerous studies have demonstrated that plant species diversity enhances ecosystem functioning in terrestrial ecosystems, including diversity effects on insects (herbivores, predators and parasitoids) and plants. However, the effects of increased plant diversity across trophic levels in different ecosystems and biomes have not yet been explored on a global scale. Through a global meta-analysis of 2,914 observations from 351 studies, we found that increased plant species richness reduced herbivore abundance and damage but increased predator and parasitoid abundance, predation, parasitism and overall plant performance. Moreover, increased predator/parasitoid performance was correlated with reduced herbivore abundance and enhanced plant performance. We conclude that increasing plant species diversity promotes beneficial trophic interactions between insects and plants, ultimately contributing to increased ecosystem services.

Allelopathy confers an invasive Wedelia higher resistance to generalist herbivore and pathogen enemies over its native congener.

The Novel Defense Hypothesis predicts that introduced plants may possess novel allelochemicals which act as a defense against native generalist enemies. Here, we aim to test if the chemicals involved in allelopathy in the invasive plant Wedelia trilobata can contribute to higher resistance against generalist herbivore and pathogen enemies by comparing with its native congener W. chinensis in controlled laboratory conditions. The allelopathic effects of the leaf extract from W. trilobata on the generalist enemies were also assessed. We showed that the larvae of two moth species preferred W. chinensis over W. trilobata. The growth rate of larvae feeding on W. trilobata leaves was significantly lower than those feeding on W. chinensis leaves. When detached leaves were inoculated with phytopathogens, the infected leaf area of W. trilobata was significantly smaller than that of W. chinensis. In addition, the leaf extract of W. trilobata also effectively inhibited the growth of the larvae and the mycelial growth of the phytopathogens. Our results indicate that the defenses of invasive W. trilobata against generalist herbivore and pathogen enemies are stronger than that of its native congener, which may be attributed to the allelopathic effects. This study provides novel insights that can comprehensively link the Novel Defense, Behavioral Constraint and Enemy Release hypotheses. These combined hypotheses would explain how invasive plants escape from their natural specialist enemies, where their allelopathic chemicals may deter herbivorous insects and inhibit pathogen infection.

Increasing plant diversity with border crops reduces insecticide use and increases crop yield in urban agriculture.

Urban agriculture is making an increasing contribution to food security in large cities around the world. The potential contribution of biodiversity to ecological intensification in urban agricultural systems has not been investigated. We present monitoring data collected from rice fields in 34 community farms in mega-urban Shanghai, China, from 2001 to 2015, and show that the presence of a border crop of soybeans and neighboring crops (maize, eggplant and Chinese cabbage), both without weed control, increased invertebrate predator abundance, decreased the abundance of pests and dependence on insecticides, and increased grain yield and economic profits. Two 2 year randomized experiments with the low and high diversity practices in the same locations confirmed these results. Our study shows that diversifying farming practices can make an important contribution to ecological intensification and the sustainable use of associated ecosystem services in an urban ecosystem.

Identification of HSP70 gene in Corythucha ciliata and its expression profiles under laboratory and field thermal conditions.

Previous laboratory studies have demonstrated that insects can tolerate high temperatures by expressing inducible heat shock proteins (HSPs). This HSP-based tolerance, however, has seldom been studied under field conditions. Here, we cloned the HSP70 gene of Corythucha ciliata (Cchsp70), an invasive insect species with substantial thermal tolerance in subtropical China. We also compared the relative mRNA expression levels of Cchsp70 in response to controlled temperature treatments (2 h at 33-43 °C at 2 °C intervals in the laboratory) and to natural increases in temperature (08:00-14:00 at 2-h intervals, 29.7-37.2 °C) on a hot summer day in the field. The complete cDNA of Cchsp70 is 2256 bp long and has a 1917 bp open reading frame that encodes a protein (CcHSP70) with 639 amino acids. The expression levels of Cchsp70 significantly increased in response to high temperatures in both laboratory and field. At similar temperatures, however, the expression levels were much higher in the field than in the laboratory. These results suggest that CcHSP70 contributes to the thermal tolerance of C. ciliata and that factors in addition to thermal stress may induce Cchsp70 expression in the field.

Spring warming increases the abundance of an invasive specialist insect: links to phenology and life history.

Under global warming, shifts in phenological synchrony between insects and host plants (i.e., changes in the relative timing of the interaction) may reduce resource availability to specialist insects. Some specialists, however, can flexibly track the shifts in host-plant phenology, allowing them to obtain sufficient resources and therefore to benefit from rising temperatures. Here, we investigated the effects of experimental warming on the life history of an invasive, specialist lace bug (Corythucha ciliata) and on the leaf expansion of its host plant (Platanus × acerifolia) in two spring seasons under field conditions in Shanghai, China. We found that a 2 °C increase in mean air temperature advanced the timing of the expansion of host leaves and of the activities of overwintering adult insects in both years but did not disrupt their synchrony. Warming also directly increased the reproduction of overwintering adults and enhanced the development and survival of their offspring. These results indicate that C. ciliata can well track the earlier emergence of available resources in response to springtime warming. Such plasticity, combined with the direct effects of rising temperatures, may increase the insect's population size and outbreak potential in eastern China under climate warming.

Acanthotomicus sp. (Coleoptera: Curculionidae: Scolytinae), a New Destructive Insect Pest of North American Sweetgum Liquidambar styraciflua in China.

A previously unknown bark beetle species, Acanthotomicus sp., has emerged as a lethal pest of American sweetgum (Liquidambar styraciflua) in China. Our survey of nursery records from around Shanghai suggests that American sweetgum have been under heavy attack since at least 2013, resulting in the death of > 10,000 trees. Mass attacks of the apparently sweetgum-specific Acanthotomicus sp. can be diagnosed by accumulation of resinous exudates on the trunk, wilted foliage, and eventual numerous exit holes of the new generation. A Chinese native sweetgum Liquidambar formosana can also be colonized by Acanthotomicus sp. This pest is of concern not only as a killer of sweetgum in the Chinese nursery trade but also as a potentially destructive invasive pest of sweetgum in North America. This discovery suggests that global preinvasion assessment of pests is warranted.

The population genetic structure of Corythucha ciliata (Say) (Hemiptera: Tingidae) provides insights into its distribution and invasiveness.

Corythucha ciliata (Say), an invasive pest originating from North America, causes severe damage on sycamore trees. However, little is known about the population genetics and evolutionary forces underlying the invasiveness of this important pest. In the present study, we use three mitochondrial genes (COI, ND1 and ND5) and nine microsatellite markers to investigate the population genetics of C. ciliata and retrace its spread through China. The results suggest a low level of genetic diversity in Chinese and European populations of C. ciliata. Our results indicate that populations of C. ciliata have obvious genetic structure, and genetic differentiation is not caused by geographic isolation. In median-joining networks, we observed a higher frequency of shared haplotypes in groups 1 and 3. Based on gene flow and approximate Bayesian computation analyses, we discovered that C. ciliata first invaded the east coast of China and subsequently moved inland. Demographic analysis suggested that populations of C. ciliata in China may have undergone a recent bottleneck effect. Finally, our results suggest that population structure, high gene flow and environmental conditions have favored the broad invasiveness of this important pest.

Increases in both temperature means and extremes likely facilitate invasive herbivore outbreaks.

Although increases in mean temperature (MT) and extreme high temperature (EHT) can greatly affect population dynamics of insects under global warming, how concurrent changes in both MT and EHT affect invasive species is largely unknown. We used four thermal regimes to simulate the increases in summer temperature and compared their effects on the life-history traits of three geographical populations (Chongqing, Wuhan and Shanghai) of an invasive insect, Corythucha ciliata, in China. The four thermal regimes were control (i.e., natural or ambient), an increase in MT (IMT), an increase in EHT, and a combination of IMT + EHT. We found that the three warming regimes significantly increased the developmental rate but did not affect the survival, sex ratio, longevity, or fecundity of C. ciliata. Consequently, the intrinsic rate of natural increase (rm) was enhanced and the number of days required for population doubling (t) was reduced by the warming regimes. The demographic parameters did not significantly differ among the three populations. These results indicate that population size of C. ciliata may be enhanced by increases in both temperature means and extremes. The increases in summer temperature associated with climate change, therefore, would likely facilitate population outbreaks of some thermophilic invasive insects.

Physiological responses of Corythucha ciliata adults to high temperatures under laboratory and field conditions.

Under high temperature conditions, insects can tolerate to survive through various physiological mechanisms, which have been well documented in laboratory studies. However, it is still unclear as to whether these laboratory data can scale up to those in the field. Here we studied dynamics of heat-induced metabolites in Corythucha ciliata adults under both laboratory and field conditions to examine their significance in thermal tolerance of the species. We compared the effects of controlled thermal treatments (2h at 33-43 °C at 2 °C intervals in the laboratory) and naturally increasing thermal conditions (10:00-14:00 at 2-h intervals (33.5-37.2 °C) on a hot summer day in a field in Shanghai, China) on water content and levels of water-soluble protein, triglycerides, mannitol, and sorbitol in the adult bodies. The results showed that water content significantly decreased and all other metabolic parameters significantly increased in response to temperature stresses with similar patterns in both the laboratory and field, although the respective threshold temperatures were different under the two conditions. The close linkage observed in the two conditions suggests that a short period of heat stress induces water loss and accumulation of thermal metabolites in C. ciliata adults. This heat-resistance provides a defense mechanism counteracting thermal damage in C. ciliata.

Anaerobic respiration and antioxidant responses of Corythucha ciliata (Say) adults to heat-induced oxidative stress under laboratory and field conditions.

High temperature often induces oxidative stress and antioxidant response in insects. This phenomenon has been well documented under controlled laboratory conditions, but whether it happens under fluctuating field conditions is largely unknown. In this study, we used an invasive lace bug (Corythucha ciliata) as a model species to compare the effects of controlled thermal treatments (2 h at 33-43 °C with 2 °C intervals in the laboratory) and naturally fluctuating thermal conditions (08:00-14:00 at 2-h intervals (29.7-37.2 °C) on a hot summer day in a field in Shanghai, China) on lipid peroxidation (malondialdehyde (MDA) was the marker) and anaerobic respiration (lactate dehydrogenase (LDH) was the marker), as well as superoxide dismutase (SOD), catalase (CAT), glutathione (GSH), and glutathione reductase (GR). The results show that MDA concentration increased significantly in response to heat stresses with similar trend in the laboratory and field. LDH activities did not significantly vary across temperatures in the laboratory-exposed individuals, but they significantly increased by rising temperature in the field. The activities or concentrations of SOD, CAT, GSH, and GR all significantly increased with increasing temperature in the two populations. These findings indicate that high temperature induces oxidative stress, resulting in high anaerobic respiration and antioxidant defenses in C. ciliata under both the laboratory and field conditions, which likely provide a defense mechanism against oxidative damage due to the accumulation of ROS.

Tolerance to high temperature extremes in an invasive lace bug, Corythucha ciliata (Hemiptera: Tingidae), in subtropical China.

Biological invasions are predicted to be more frequent as climate change is increasing its positive impact on the prevalence of invasive exotic species. Success of insect invaders in different temperature zones is closely related to their tolerance to temperature extremes. In this study, we used an exotic lace bug (Corythucha ciliata) as the study organism to address the hypotheses that an insect species invading a subtropical zone from temperate regions has a high capacity to survive and adapt to high temperatures, and that its thermal tolerance plays an important role in determining its seasonal abundance and geographic distribution. To test these hypotheses, the effects of heat shock on the survival and reproduction of C. ciliata adults were assessed in the laboratory. Adults were exposed to 26 (control), 35, 37, 39, 41, 43, and 45°C for 2 h, and then were transferred to 26°C. Heat-shock temperatures ranging from 35 to 41°C did not significantly affect survival pattern, longevity, and fecundity of adults, but heat shock at 43 and 45°C significantly reduced these traits. Exposing parent females to heat-shock treatments from 35 to 41°C did not significantly affect the hatching rate of their eggs, survival of the nymphs, and the proportion of female F(1) progeny, while no progeny were produced with treatments of 43 and 45°C. The results indicate that C. ciliata can tolerate high temperatures less than 41°C, which may contribute to its expansion into the lower latitudes in China where its hosts (Platanus trees) are widely planted. Our findings have important implications for predicting seasonal abundance and understanding invasion mechanisms of this important urban invader under climate change.

Rapid cold hardening increases cold and chilling tolerances more than acclimation in the adults of the sycamore lace bug, Corythucha ciliata (Say) (Hemiptera: Tingidae).

The sycamore lace bug, Corythucha ciliata is a new, invasive pest of Platanus trees in China. Although C. ciliata is often subjected to acute low temperatures in early winter and spring in northern and eastern China, the cold tolerance of C. ciliata has not been well studied. The objectives of this study were to determine whether adults of C. ciliata are capable of rapid cold hardening (RCH), and to compare the benefits of RCH vs. cold acclimation (ACC) in the laboratory. When the adult females incubated at 26°C were transferred directly to the discriminating temperature (-12°C) for 2 h, survival was only 22%. However, exposure to 0°C for 4 h before transfer to -12°C for 2 h induced RCH, i.e., increased survival to 68%. RCH could also be induced by gradual cooling of the insects at rates between 0.1 and 0.25°C min(-1). The protection against cold shock obtained through RCH at 0°C for 4 h was lost within 1h if the adults were returned to 26°C before exposure to -12°C. Survival at both -12 and -5°C was greater for RCH-treated than for ACC-treated adults (for ACC, adults were kept at 15°C for 5 days), and the lethal temperature (2 h exposure) was lower for RCH-treated than for ACC-treated adults. The results suggest that RCH may help C. ciliata survive the acute low temperatures that often occur in early winter and early spring in northern and eastern China.

Effects of temperature on the development and population growth of the sycamore lace bug, Corythucha ciliata.

The sycamore lace bug, Corythucha ciliata (Say) (Hemiptera: Tingidae), is an important invasive exotic pest of Platanus (Proteales: Platanaceae) trees in China. The objective of this study was to determine the effects of temperature on C. ciliata in the laboratory so that forecasting models based on heat accumulation units could be developed for the pest. Development and fecundity of C. ciliata reared on leaves of London plane tree (Platanus × acerifolia) were investigated at seven constant temperatures (16, 19, 22, 26, 30, 33, and 36° C) and at a relative humidity of 80% with a photoperiod of 14:10 (L:D). The developmental time was found to significantly decrease with increasing temperature. The developmental time from egg hatching to adult emergence was respectively 47.6, 35.0, 24.1, 20.0, and 17.1 days at the temperatures of 19, 22, 26, 30, and 33° C. C. ciliata could not complete full development at 16° and 36° C. The developmental threshold temperature (C) estimated for egg-to-adult was 11.17° C, with a thermal constant of (K) 370.57 degree-days. Longevity of females was found to be the shortest, 17.7 days at 33° C and the longest, 58.9 days at 16° C, and that of males was the shortest, 19.7 days at 33° C and the longest, 59.7 days at 16° C. Fecundity was the highest at 30° C, being 286.8 eggs per female over an oviposition period of 8.9 days. Female lifetime fecundity was reduced at other temperatures, being the lowest (87.7 eggs per female) at 19° C. The population trend index (I) of C. ciliata was the highest (130.1) at 30° C and the lowest (24.9) at 19° C. Therefore, the optimal developmental temperature for C. ciliata was determined to be 30° C.

Supercooling capacity and cold hardiness of the adults of the sycamore lace bug, corythucha ciliata (Hemiptera:Tingidae).

Supercooling point (SCP) of female adults of Corythucha ciliata was significantly lower than that of male adults, with an average being -11.49 degrees C and -9.54 degrees C, respectively. Low temperature survival of adults of different ages indicated that there were differences in cold survival ability among age groups of adults. Nonlinear regression analysis found that the response of C. ciliata adults to exposure time under different low temperature regimes (above -5 degrees C) was best fitted by a logistic equation. Both low temperature and exposure time had significant effects on mortality of adults. Temperatures above 5 degrees C did not prevent C. ciliata adults from surviving. C. ciliata was shown to be a freeze-intolerant but chill-tolerant insect. C. ciliata could tolerate subzero temperatures by supercooling. Temperature around -8 degres C is a critical point for successful overwintering of C. ciliata adults, which can establish in the whole areas where Platanus trees are planted in China.

[Effects of host plants on development and fecundity of Brontispa longissima (Gestro)].

With Cocos nucifera, Hyophorbe lagenicaulis, Washingtonia filifera, Roystonea regia and Areca catechu as test host plants, this paper studied the effects of their un-spread leaves on the development and fecundity of experimental population of Brontispa longissima. The results showed that the development duration of one generation B. longissima fed on different hosts varied significantly, with the longest (72.8 days) on W. filifera and the shortest (39.8 days) on H. lagenicaulis. The average pupa weight of B. longissima was bigger on H. lagenicaulis than on the other four host plants, and the female B. longissima had the highest fecundity (157.6 ova) on W. filifera while the lowest one (65.2 ova) on A. catechu. The longevity of B. longissima adults fed on H. lagenicaulis was 207.52 days, being significantly longer than that on the other host plants. The trend index of experimental population of B. longissima fed on the five host plants was 53.57, 54.98, 48.56, 20.46 and 11.54, respectively.