American fall webworm in China: A new case of global biological invasions

Abstract

Season of mists and mellow fruitfulness—a wonderful autumn scene was described by the poet John Keats. Unfortunately, in multiple locations in China, this picturesque scenery has been nibbled away by an invasive insect, fall webworm, Hyphantria cunea (Lepidoptera: Arctiidae). By the end of September in 2021, outbreaks were detected in 607 counties in 14 provinces, resulting in cumulative damage of 10,427,300 acres and increasing the amount of infested area by 6.15% than last year (Data from Biological Disaster Prevention and Control Center, China). Fall webworm is native to North America, but during the past 80 years, it has become highly invasive throughout the Northern Hemisphere (Figure 1A ). In China, the pest was invaded to Liaoning province in 1979, after which it has expanded its range rapidly and caused unprecedented economic losses.1Wu N.N. Zhang S.F. Li X.W. et al.Fall webworm genomes yield insights into rapid adaptation of invasive species.Nat. Ecol. Evol. 2019; 3: 105-115Crossref PubMed Scopus (30) Google Scholar,2Tang R. Zhang J.P. Zhang Z.N. Electrophysiological and behavioral responses of male fall webworm moths (Hyphantria cunea) to herbivory-induced mulberry (Morus alba) leaf volatiles.PLoS ONE. 2012; 7: e49256Crossref PubMed Scopus (25) Google Scholar The robust adaptability of fall webworm results from its high polyphagy and reproductive capability. It can feed on about 600 species of deciduous trees worldwide. The preferred host plants include multiple globally important tree species, such as mulberry, oak, hickory, pecan, walnut, elm, alder, and poplar.1Wu N.N. Zhang S.F. Li X.W. et al.Fall webworm genomes yield insights into rapid adaptation of invasive species.Nat. Ecol. Evol. 2019; 3: 105-115Crossref PubMed Scopus (30) Google Scholar, 2Tang R. Zhang J.P. Zhang Z.N. Electrophysiological and behavioral responses of male fall webworm moths (Hyphantria cunea) to herbivory-induced mulberry (Morus alba) leaf volatiles.PLoS ONE. 2012; 7: e49256Crossref PubMed Scopus (25) Google Scholar, 3Takehiko Y. Sadahiro T. Masakazu S. Adaptation to the new land or effect of global warming? An age-structured model for rapid voltinism change in an alien lepidopteran pest.J. Anim. Ecol. 2008; 77: 585-596Crossref PubMed Scopus (21) Google Scholar Genetic diversity and genome structure have played major roles in fall webworm's ability for high polyphagy. Genes and pathways associated with carbohydrate metabolism, gustatory and olfactory receptors are substantially expanded in the webworm's genome and show strong signatures of functional polymorphisms in the invasive populations.1Wu N.N. Zhang S.F. Li X.W. et al.Fall webworm genomes yield insights into rapid adaptation of invasive species.Nat. Ecol. Evol. 2019; 3: 105-115Crossref PubMed Scopus (30) Google Scholar These findings suggest that fall webworm's ability to colonize novel hosts and adapt to new environments is mediated by the plasticity in the gustatory capabilities, along with the increased ability to utilize novel nutrition sources and detoxify harmful compounds. This insect has a multivoltine life cycle, typically having two to three generations per year.3Takehiko Y. Sadahiro T. Masakazu S. Adaptation to the new land or effect of global warming? An age-structured model for rapid voltinism change in an alien lepidopteran pest.J. Anim. Ecol. 2008; 77: 585-596Crossref PubMed Scopus (21) Google Scholar An adult female can lay up to 900 eggs during each oviposition period, and due to the generation overlap, her total number of offspring may reach up to 400,000 per year.1Wu N.N. Zhang S.F. Li X.W. et al.Fall webworm genomes yield insights into rapid adaptation of invasive species.Nat. Ecol. Evol. 2019; 3: 105-115Crossref PubMed Scopus (30) Google Scholar Damage is mainly caused by the larvae, which have seven instars. After entering the fourth instar, the food intake of the larvae increases sharply: a group of larvae can defoliate an entire tree within 3 to 4 days. The gregarious smaller larvae construct a massive silk web tent as a protection against competitors and natural enemies, whereas mature larvae rely on the long bristles or hairs on their bodies for defense. Temperature tolerance affect the survival and geographic distribution range of insect. Fall webworm is highly tolerant to extreme temperatures, withstanding temperatures ranging from −16°C to 40°C. This wide thermal tolerance provides the basis for the survival of the moth in a wide range of environments. Fall webworm also adjusts the number of generations per year depending on the ambient temperature: during colder years, bivoltine populations often occur, whereas trivoltine populations are more common during warmer years.3Takehiko Y. Sadahiro T. Masakazu S. Adaptation to the new land or effect of global warming? An age-structured model for rapid voltinism change in an alien lepidopteran pest.J. Anim. Ecol. 2008; 77: 585-596Crossref PubMed Scopus (21) Google Scholar The preference of moth for high-humidity environments is supported by facts that its optimal relative humidity range is in between 70% and 80% and that the outbreaks are often correlated with high frequency of rainfall. During September in 2021, fall webworm had extensive three-generation outbreaks. Firstly, the abnormally fluctuating temperatures resulted in an irregular and extended (from mid-April until late June) emergence pattern of the first adult generation. Such pattern may have prolonged the oviposition period, resulting in wider generation overlaps and higher larval abundance (Figure 1D). Secondly, the 15 rainy days more than doubled September's average precipitation, which promoted the growth and development of the third larva generation (Figures 1B, 1C, and 1E). In brief, the stronger weather fluctuation caused the third generation of fall webworm to break out in a short period of time. Climate change and invasive species influence ecosystem functions and may enhance each other's negative impacts. Global warming is expected to increase the frequency of extreme weather events, which may facilitate the propagation and spread of invasive species,3Takehiko Y. Sadahiro T. Masakazu S. Adaptation to the new land or effect of global warming? An age-structured model for rapid voltinism change in an alien lepidopteran pest.J. Anim. Ecol. 2008; 77: 585-596Crossref PubMed Scopus (21) Google Scholar, 4Diagne C. Leroy B. Vaissière A.C. et al.High and rising economic costs of biological invasions worldwide.Nature. 2020; 592: 571-585Crossref Scopus (71) Google Scholar, 5Wang D. Liu X. Behavioral innovation promotes alien bird invasions.The Innovation. 2021; 2: 100167Abstract Full Text Full Text PDF PubMed Google Scholar which generally are highly adaptable to various environments. Climate change may also reduce habitats' resilience against biological invasions by reducing biodiversity. Invasive species, in turn, can reduce the resilience of natural habitats, agricultural systems, and urban areas against climate change by interfering with ecosystem functions. The costs of invasive alien species and their management are high, with the total reported costs reaching minimum US $1.288 trillion over the past decades (1970–2017), up to US $162.7 billion in 2017.4Diagne C. Leroy B. Vaissière A.C. et al.High and rising economic costs of biological invasions worldwide.Nature. 2020; 592: 571-585Crossref Scopus (71) Google Scholar,5Wang D. Liu X. Behavioral innovation promotes alien bird invasions.The Innovation. 2021; 2: 100167Abstract Full Text Full Text PDF PubMed Google Scholar Therefore, interdisciplinary subjects, such as bioclimate and biometeorology, have become new research hotspots that will hopefully aid our understanding of the role of climate change in species invasion. In China, climate change will likely increase habitat suitability for fall webworm in middle and high latitude regions. Human mobility and logistics also increase the risk of spread of the pest to new areas. The eastern farmland and man-made vegetation regions are high risk areas mainly in Liaoning, Beijing, Tianjin, Shanghai, Hebei, Shandong, Henan, Anhui, Hubei, Jiangsu, and Shanxi. Fall webworm is also threating to spread to Jilin, Inner Mongolia, Hunan, Jiangxi, Xinjiang, Ningxia, and other provinces. This work was supported by National Key Plan for Scientific Research and Development of China ( 2021YFC2600100 ), Basic Frontier Scientific Research Program of the Chinese Academy of Sciences from 0 to 1 ( ZDBS-LY- SM027-03 ), Strategic Priority Research Program of Chinese Academy of Sciences (Grant No. XDPB16 ). The authors declare no competing interests.

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