Perspectives of invasive alien species management in <scp>C</scp>hina

Abstract

Biological invasions pose a significant threat to ecosystems, resulting in substantial negative ecological, environmental, and economic impacts globally (Diagne et al., 2021; Pyšek et al., 2020). China is one of the countries significantly affected by invasive alien species (IAS) and, unfortunately, the impacts of biological invasions have not shown any signs of decline due to increasing anthropogenic activities such as sustainable globalization (Ding et al., 2008; Du et al., 2023; Li & Ma, 2010; Lin et al., 2015; Liu et al., 2022; Wan et al., 2017). Understanding the risks, mechanisms, performances, and impacts of IAS in China is critically important to the development of effective management strategies such as control and mitigation. In this special feature, we publish 24 papers focusing on these topics (Figure 1), covering a wide range of subjects related to the management of IAS across plants, invertebrates, and vertebrates in China. These studies used diverse methods including eDNA techniques, mesocosm experiments, field surveys, and ecological modeling to assess invasion risks and investigate mechanisms based on various hypotheses of environmental filter, biotic interaction, adaptive evolution, phenotypic plasticity, habitat feedback and clonal process, invaders' performance from their advantages in competition, reproduction, and growth compared with natives, impacts mainly for plant invaders from leaf litter decomposition and soil feedback, and control strategies derived from native biotic resistance and additional eradications. A Chinese-language summary of the special feature is provided in Appendix S1. Quantifying the invasion risk of IAS at early stages is crucial for developing timely and effective prevention and eradication strategies. In this special feature, four studies used multidisciplinary approaches, including molecular eDNA techniques, macroecological predictive models, and online trade tools, to examine the invasion risk posed by alien invertebrates, vertebrates, and plants in China. Water diversions linking different biogeographic regions create “invasion highways” in aquatic ecosystems. The use of eDNA has gained increasing popularity as an effective high-throughput approach for detecting aquatic IAS. Following the opening of the South-to-North Water Diversion Project, Xia et al. (2023) conducted intensive field eDNA surveys to assess the invasion risk of the golden mussel (Limnoperna fortune), an invasive biofouling bivalve, in this world's largest water diversion project. Their findings established an “eDNA concentration-flowing distance” relationship, confirming the creation of an “invasion highway” that facilitated the spread of this invader to the northern invasion front. They also identified a key control period to reduce further spread and mitigate negative impacts. Wang, Xu, et al. (2023) also focused on this invasive mussel and investigated the environmental variables responsible for the survival of veligers at different developmental stages in the invasion front in Beijing. Their study showed that controlling early-stage veligers through adjustments in water temperature, pH, and food size could effectively limit further spread. Protected areas (PAs) are considered the cornerstone of biodiversity conservation, but they face threats from invasive species. Despite this, the risk has not been evaluated under current and future global change scenarios. Xin et al. (2023) applied ecological niche modeling to investigate the risk of alien vertebrate establishment and overlapped the predicted habitat suitability with climate change and land-use modifications in a total of 1020 terrestrial PAs with clear geographic boundaries and varying functions in China. Their findings indicated that more than half of the PAs were predicted to face at least one stress factor, and specifically many wildlife conservation PAs could provide suitable habitats for the establishment of feral populations of alien vertebrate species, emphasizing the need for early prevention schemes in PAs with high invasion potentials. The burgeoning trend of e-commerce has significantly impacted the horticulture sector, leading to an increase in the online trade of plants with invasive potentials. China, currently grappling with 933 established (214 invasive) plant species primarily introduced for cultivation, exemplifies this concern. These species, frequently traded online, continue to increase invasion risks. Through a synthesis evaluation, Dong et al. (2023) found that naturalized noninvasive and invasive plant taxa were more likely to be available for purchase. The implementation of stringent plant trading regulations and monitoring of online horticulture supply chains is urgently needed to mitigate the further spread of these invasive species. Exploring mechanisms of invasion success is of fundamental importance to develop and implement management strategies for IAS. In this collection, a total of 15 papers delved into invasion mechanisms using field observations, experimental studies, and genomics methods. Key functional traits, such as clonal integration, are often associated with the invasiveness of IAS, especially in the context of global environmental changes. Wang, Liu, et al. (2023) discovered that clonal integration significantly contributed to the success of alien plants, particularly in low-density communities with limited species diversity or increased nutrient availability. Their findings also revealed a negative correlation between the invasion success and resistance of native communities along changing environmental gradients. While local adaptation and phenotypic plasticity in functional traits are potential influencers of the invasiveness of alien plants, their relative contributions remain uncertain. According to Xiong et al. (2023), adaptive evolution and phenotypic plasticity in various traits may work in synergy to enhance the invasiveness of Ambrosia artemisiifolia in China under varying nitrogen levels. Their results showed that both phenotypic plasticity and rapid adaptive evolution could enable invasive plants to thrive across diverse environmental conditions. Phenotypic plasticity can also extend across generations, a phenomenon known as transgenerational plasticity, which has not been well understood. Liu et al. (2023) conducted measurements of plant morphology, aboveground parts, and growth across three generations of invasive Xanthium strumarium in northeast China. They identified stronger intergenerational plasticity under stress conditions, with both water and nutrients playing pivotal roles in influencing the intergenerational transmission of plasticity. These findings contribute to our understanding of the link between the invasion process and key traits of transgenerational plasticity. Rapid adaptive evolution is typically associated with genetic and epigenetic changes, but the interplay between these two components underlying rapid adaptation in invasive species remains unclear. Chen et al. (2023) found that the complementary interplay of genetic and epigenetic variation was involved in the local adaptation of a marine invasive model ascidian (Ciona intestinalis). This complementary interplay collectively promoted the rapid adaptive capacity of populations, enabling successful invasions in different environments. These findings offer valuable insights into the interactions between invasive species and local environments, enabling them to colonize and spread rapidly. From a biogeographical perspective, understanding the role of climate change and human activities in driving the distribution of alien species is crucial for predicting adaptive capabilities and future invasion potentials. A study by Hu and Dong (2023) on the marine species Crassostrea sikamea demonstrated that the rapid northward expansion of the southern population, in response to climate change and coastal development, was facilitated by multiple sources of divergent thermal adaptability. These findings provide valuable insights into the genetic origins and dispersal mechanisms of intertidal oysters during their northward shift along China's coast, highlighting the importance of rapid adaptation to local environments in driving distribution shifts and preserving population viability at the distribution edge. Biotic interactions between IAS and native species play a crucial role in determining the success of IAS. One prominent hypothesis, the invasional meltdown hypothesis, suggests that an initial invasive species can facilitate secondary invasions, and the potential underlying mechanisms are likely derived from modifications of soil properties by the initial invaders, thus promoting subsequent exotic species invasions. Li and Xu (2023) found that Rhus typhina invasions significantly altered the composition of soil fungal communities, while this change in microbial composition led to neither direction nor magnitude changes in negative plant–soil feedback effects on both native and invasive species. These findings challenge the invasional meltdown hypothesis by indicating that the initial invasion of R. typhina did not facilitate subsequent herb invasions. Conversely, the enhanced mutualism hypothesis posits that invasive plants promote their own growth by enriching beneficial microbes in the soil, thereby establishing positive soil feedback. Meng et al. (2023) found that plant growth-promoting bacteria accumulated significantly in the soil during the early stages of Phytolacca americana invasions, and in turn the strength of enhanced positive feedback was likely to have facilitated P. americana invasions. This study highlights the evolving nature of plant–microbe interactions during biological invasions and underscores the role of bacteria in the initial success of P. americana invasions. In addition to these hypotheses, the apparent competition hypothesis emphasizes the idea that the evolutionary naivety of native plants to alien herbivores can render them more susceptible to the detrimental effects of herbivory compared to co-occurring invasive plants. Yan et al. (2023) provided support for this hypothesis in a lake ecosystem, where the co-invasions of the alien snail Pomacea canaliculata and macrophyte that come from the same biogeographic region and possibly share evolutionary history can be detrimental to the recipient native macrophyte community in the lake ecosystem. Disturbed habitats are widely recognized contributors to the success of invasive species by providing vacant niches. Le et al. (2023) conducted field surveys to investigate the correlation between the distribution of alien plants and habitat characteristics in the Three Gorges Reservoir Area (TGRA) of China. Their study revealed that this large-scale water conservancy project could indeed facilitate invasions by altering hydrological regimes. Furthermore, their results indicated that the richness of alien species decreased as native biodiversity increased, thus supporting the biotic resistance hypothesis. This highlights the importance of conserving native species in TGRA to resist the encroachment of alien plants. Numerous studies have linked geomorphic landscape features, such as tidal channels, to invasions by exotic plants. However, the role of tidal channel meanders, specifically the convex and concave sides, in regulating the invasion of Spartina alterniflora, remains unclear. Ning et al. (2023) found that lower hydrodynamic disturbance and bed shear stress, coupled with higher propagule pressure triggered by eddies due to the convex structure of channel meanders, facilitated Spartina seedling establishment and growth. These findings demonstrate that the meandering geomorphic structures of tidal channels could act as stepping stones to significantly facilitate the landward invasions of Spartina along tidal channels. Understanding why some communities are more readily invaded than others is a primary goal of invasion ecology and conservation biology. The study by Gu et al. (2023) supported the biotic resistance hypothesis in freshwater ecosystems and suggested that protecting freshwater fish diversity is an important and effective pathway to mitigate the impacts of alien fishes. Some successful invaders generally exhibit higher performances than native species. The enemy release hypothesis suggests that invasive alien plants, due to a growth–defense trade-off, often demonstrate superior growth and weaker antiherbivory defenses compared with native plants. Shan et al. (2023) conducted a multispecies greenhouse experiment to examine how nutrient enrichment in invaded habitats influenced this growth–defense trade-off between invasive and co-occurring native plants. Their study revealed that invasive species, relative to native ones, displayed an enhanced ability to adjust their flavonoid-based defenses in response to shifts in soil nutrient availability and herbivory pressure. This adaptive ability enhanced their invasiveness under conditions of nutrient enrichment. These findings have important implications for the control of invasive alien plants in China, emphasizing the potential benefits of reducing habitat nutrient enrichment. Furthermore, temporal fluctuations in nutrient availability can promote the growth of invasive alien plants and further invasions. However, the effects of fluctuating nutrients on invasive species remain unclear, particularly in the context of varying habitat resources under global change. Using six plant invaders and six other native plants in a pot experiment system, Otieno et al. (2023) found that the impact of fluctuating nutrient availability on the growth of plant invaders was strongly dependent on the variations in water resources. This study provides valuable insights into the management of invasive plants in changing environments. Additionally, Tao et al. (2023) revealed diverse responses to nutrient pulses among alien species, with certain species gaining advantages while others did not. Importantly, in a community context, nutrient fluctuations promoted the success of advantaged species. Given the prevalence of resource fluctuation in natural habitats, considering resource fluctuation is crucial for predicting the outcomes of interactions among alien species. The role of ploidy levels in plant invasiveness has long been a subject of interest, yet the findings remain inconclusive. Using the intricate autopolyploid invasive species Solidago canadensis as a case study, Feng et al. (2023) determined that polyploidization fostered effective clonal growth through preadaptation and postintroduction evolution. As a result, controlling clonal reproduction emerges as a critical factor in managing S. canadensis invasions. In addition to the traditional impacts, such as competition, predation, and disease transmission, IAS can also influence key ecological processes during their invasions. For example, Cheng et al. (2023) conducted field surveys across a wide 18° latitudinal range and a 90-day incubation experiment. They found that variations existed in leaf litter decomposition and its dominant controlling factors between native and invaded plant communities. Disentangling these biogeographic patterns and key drivers of soil organic matter (SOM) decomposition and its temperature sensitivity under plant invasion is crucial for projecting global carbon feedback. Zhang et al. (2023) found inconsistent responses to invasion among habitat types, with SOM accumulation in salt marshes but carbon loss in mangroves. These variations were at least partially explained by the patterns of SOM decomposition under invasions. These findings shed light on the geographic patterns of SOM decomposition and its temperature sensitivity in coastal ecosystems, emphasizing the importance of interactions between climate, soil, and microbiota in stabilizing SOM under plant invasions. The soil seed bank plays a vital role in community restoration and species diversity protection. Jia et al. (2023) discovered that soil seed banks potentially played important roles in the restoration of depredated coastal salt marsh wetlands. These results provide valuable insights for evaluating the ecological impacts of S. alterniflora invasions in eastern China's coastal salt marsh wetlands and offer guidance for the protection and restoration of native plant communities. The impact of IAS may vary with control actions. For instance, the rehabilitation of diverse communities and trophic interactions following the removal of invasive plants is a crucial goal of ecological restoration. Jiang et al. (2023) found that although S. alterniflora invasions had altered arthropod diversity, trophic structure, and diets in saltmarshes, these changes could be reversed through the restoration of native Phragmites. These findings highlight the positive effects of controlling invasive plants on biodiversity and nutrient cycling in salt marsh ecosystems. Furthermore, several studies have explored the mitigation effect and underlying mechanisms of biochar (IBC) and its composite with hydroxyapatite (HAP) to address negative allelopathy from invasive plants. Xu et al. (2023) discovered that the HAP/IBC composite could more effectively mitigate allelopathy from invasive S. canadensis than IBC, which may be a potentially efficient approach to control the invasive plant and improve invaded soils. Their findings indicate that the environmentally friendly composite HAP/IBC may have potential ecological applications in preventing and controlling invasive plants and the restoration of local plant communities in China. There is no doubt that the rates of biological invasions continue to accelerate, posing increasingly urgent and destructive impacts on the global environment and economy. In China, the central, regional, and local governments have prioritized the management of biological invasions, and such prioritization has largely promoted studies on the causes and consequences of biological invasions. The development and successful implementation of effective management strategy needs interdisciplinary comprehensive studies at various spatial–temporal scales to understand the risks, mechanisms, performances, and impacts of IAS across taxonomic groups at different invasion stages. This special feature addresses these critical questions through a range of approaches, including field surveys, experiments, ecological modeling, and molecular techniques, conducted across diverse terrestrial and aquatic ecosystems, and further explores strategies for controlling and mitigating invasive species based on scientific insights derived from theoretical investigations. All the articles published in this special feature provide valuable insight into future basic and applied studies in IAS in China under the continued globalization. No data were collected for this study. Appendix S1. Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.

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