Introduced plants induce outbreaks of a native pest and facilitate invasion in the plants’ native range: Evidence from the emerald ash borer

Metadata:
Identification_Information:
Citation:
Citation_Information:
Originator: Dang, Yingqiao
Originator: Wei, Ke
Originator: Wang, Xiaoyi
Originator: Duan, Jian J.
Originator: Jennings, David E.
Originator: Poland, Therese M.
Publication_Date: 2021
Title:
Introduced plants induce outbreaks of a native pest and facilitate invasion in the plants’ native range: Evidence from the emerald ash borer
Geospatial_Data_Presentation_Form: spreadsheet
Series_Information:
Series_Name: Dataset
Publication_Information:
Publisher: Dryad
Online_Linkage: https://doi.org/10.5061/dryad.8gtht76qn
Description:
Abstract:
Biological invasions are among the most serious threats to native forest ecosystems worldwide due to ever-increasing international trade and global change. Understanding the invasion processes and ecology of invasive pests in both newly invaded and native habitats is necessary to effectively manage the risks they pose. The emerald ash borer (EAB), Agrilus planipennis, is one of the most devastating invasive forest insect pests in North America and has also invaded European Russia and parts of Europe. Through synthesizing historical data spanning >100 years and contemporary field observations in China, we examined EAB’s distribution, occurrence, and outbreak frequency in its native range in relation to historical introductions and plantings of non-Asian ash trees in China. The frequencies and levels of EAB infestations in China gradually increased from 1900 to 2021 after a time-lag of 30-50 years following introductions and widespread plantings of non-Asian ash trees from North America. Increased frequencies of EAB outbreaks following the planting of North American ash trees in China may have increased the risk of EAB invading North America and other novel regions. Our findings demonstrated that planting susceptible non-native host plants can induce outbreaks of a native insect pest in its native range, which in turn may enhance risks of invading novel regions via human-assisted activities (e.g., international trade). In addition, our findings suggest that lag-times of several decades between planting susceptible hosts and initial pest outbreaks may pose challenges in predicting the true risk of invading novel regions. Consequently, comprehensive risk assessment for invasive insect pests should consider the role of non-native plants introduced or planted in the pest’s native range.
Purpose:
The purpose of this study was to examine EAB’s distribution, occurrence, and outbreak frequency in its native range in relation to historical introductions and plantings of non-Asian ash trees in China.
Supplemental_Information:
For more information about this study and these data, see Dang et al. (2021).
Time_Period_of_Content:
Time_Period_Information:
Range_of_Dates/Times:
Beginning_Date: 1961
Ending_Date: 2021
Currentness_Reference:
Ground condition
Status:
Progress: Complete
Maintenance_and_Update_Frequency: Unknown
Spatial_Domain:
Description_of_Geographic_Extent:
China
Bounding_Coordinates:
West_Bounding_Coordinate: 81
East_Bounding_Coordinate: 130
North_Bounding_Coordinate: 48
South_Bounding_Coordinate: 25
Keywords:
Theme:
Theme_Keyword_Thesaurus: ISO 19115 Topic Category
Theme_Keyword: biota
Theme:
Theme_Keyword_Thesaurus: National Research & Development Taxonomy
Theme_Keyword: Forest & Plant Health
Theme_Keyword: Insects
Theme_Keyword: Invasive species
Theme:
Theme_Keyword_Thesaurus: None
Theme_Keyword: Agrilus planipennis
Theme_Keyword: ash trees
Theme_Keyword: biological invasion
Theme_Keyword: insect-plant Interactions
Theme_Keyword: native range
Theme_Keyword: risk assessment
Place:
Place_Keyword_Thesaurus: None
Place_Keyword: China
Access_Constraints: None
Use_Constraints:
If you use these data in a publication, presentation, or other research product please use the following citation:

Dang, Yingqiao; Wei, Ke; Wang, Xiaoyi; Duan, Jian J.; Jennings, David E.; Poland, Therese M. 2021. Introduced plants induce outbreaks of a native pest and facilitate invasion in the plants’ native range: Evidence from the emerald ash borer. Dryad. Dataset. https://doi.org/10.5061/dryad.8gtht76qn
Data_Set_Credit:
We thank Dr. Rodrigo J. Mercader and Dr. Andrew M. Liebhold for their helpful comments on an earlier version of the manuscript, and Dr. John Stanovick, mathematical statistician from the USDA-Forest Service, Northern Research Station, for assistance with the data analyses. We also thank three anonymous reviewers, associate editor and professor Mark Rees, University of Sheffield, UK for their valuable suggestions and comments. This work was primarily supported by the National Key R & D Program of China (2018YFC1200400), National Natural Science Foundation of China (31971666) and Fundamental Research Funds of Chinese Academy of Forestry (CAFYBB2017ZF002). The United States Forest Service International Programs and USDA Agriculture Research Service partly supported data collection under the agreement (58-8010-7-005-F) with Chinese Academy of Forestry.


Author Information:

Dang, Yingqiao
Key Laboratory of Forest Protection of National Forestry and Grassland Administration, Research Institute of Forest Ecology, Environment and Protection, Chinese Academy of Forestry, Beijing, China
https://orcid.org/0000-0001-5349-9691

Wei, Ke
Key Laboratory of Forest Protection of National Forestry and Grassland Administration, Research Institute of Forest Ecology, Environment and Protection, Chinese Academy of Forestry, Beijing, China
https://orcid.org/0000-0001-9792-9972

Wang, Xiaoyi
Key Laboratory of Forest Protection of National Forestry and Grassland Administration, Research Institute of Forest Ecology, Environment and Protection, Chinese Academy of Forestry, Beijing, China
https://orcid.org/0000-0001-8136-6642

Duan, Jian J.
Beneficial Insects Introduction Research Unit, USDA Agricultural Research Service, Newark, DE, USA
https://orcid.org/0000-0002-8476-3480

Jennings, David E.
Vermont Law School, South Royalton, VT, USA
https://orcid.org/0000-0001-7179-3069

Poland, Therese M.
Northern Research Station, USDA Forest Service, Lansing, MI, USA
https://orcid.org/0000-0001-7684-1306
Cross_Reference:
Citation_Information:
Originator: Dang, Yingqiao
Originator: Wei, Ke
Originator: Wang, Xiaoyi
Originator: Duan, Jian J.
Originator: Jennings, David E.
Originator: Poland, Therese M.
Publication_Date: 2021
Title:
Introduced plants induce outbreaks of a native pest and facilitate invasion in the plants' native range: Evidence from the emerald ash borer
Geospatial_Data_Presentation_Form: journal article
Series_Information:
Series_Name: Journal of Ecology
Issue_Identification: 110(3): 595-604
Online_Linkage: https://doi.org/10.1111/1365-2745.13822
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Data_Quality_Information:
Attribute_Accuracy:
Attribute_Accuracy_Report:
none provided
Logical_Consistency_Report:
none provided
Completeness_Report:
none provided
Lineage:
Methodology:
Methodology_Type: Field
Methodology_Description:
Current and historical occurrences of EAB in China

To determine the recent occurrence and distribution of EAB infestations in China, we obtained data from field surveys conducted from 2003 to 2021 in 13 regions of China (Table S1 in Dang et al. 2021), as well as records from literature and reports of local faunas about the presence of EAB infestations. An EAB infestation was defined as an area with visibly damaged ash trees that displayed characteristic signs of EAB attack including D-shaped emergence holes or bark splits that form over larval galleries as a potential tree defence mechanism to expose larvae to unfavourable weather conditions or natural enemies. We considered an infestation to be at outbreak level when EAB abundance increased within a period of 1–3 years resulting in more than 50% of trees being infested.

Sample sites for field surveys included the following: (a) areas within EAB's distribution with reports of EAB infestations or outbreaks, (b) areas suspected to be within EAB's distribution with records of EAB presence which required verification by field investigation but no damage reports and (c) areas with ash tree species but no historical records of EAB presence or infestation. Sample habitats were divided into three categories: (i) street trees: trees on roadsides; (ii) plantations: trees in parks, courtyards, neighbourhoods, university campuses or nurseries; and (iii) semi-natural conditions: trees growing in natural ecosystems or natural regenerations. A total of 83 sample plots (1-ha plantation or semi-natural site, or a site with at least 400 street trees) were arbitrarily selected (Table S1 in Dang et al. 2021). In all, 30 ash trees were then randomly selected in each plot to determine the percentage of infested ash trees (n, where n = number of infested ash trees /30 × 100). The degree of EAB infestation was graded on a scale of 0–4 based on the percentage of infested ash trees (n): 0 = undamaged, with n = 0; 1 = slightly damaged, with 0 < n < 10%; 2 = moderately damaged, with 10% ≤ n < 50%; 3 = seriously damaged, with 50% ≤ n < 90%; 4 = extremely damaged, with n ≥ 90%.


Variables related to EAB occurrences in China

Seven variables, including degree of EAB infestation, host tree species, age, and size, habitat, latitude and elevation, were recorded during field surveys in 13 regions of China from 2003 to 2021. Host tree size was measured as diameter at breast height (DBH). The degree of EAB infestation was graded as described above.

From 2012 to 2013, complementary field surveys were conducted in the Oleaceae Common Garden at the Institute of Botany, Chinese Academy of Sciences (39.99°N, 116.22°E) which contained both native and non-Asian ash species. Fraxinus pennsylvanica var. lanceolata (Borkh.) Sarg. (syn. var. subintegerrima (Vahl) Fern.) was combined with F. pennsylvanica Marshall. Fraxinus excelsior var. aurea was combined with F. excelsior L. Fraxinus rhynchophylla Hance and F. chinensis rhynchophylla (=F. chinensis Roxb. subsp. rhynchophylla (Hance) A. E. Murray) were combined with F. chinensis Roxb. All of the 39 native and 71 non-Asian ash trees in the 2.5 ha Oleaceae Common Garden were investigated and the data were collected on the same seven variables as well as canopy condition, presence of bark splits and presence of EAB infestation on individual trees. Canopy condition was assigned an index on a scale with five levels based on the percentage of live crown (m): (1) m ≥ 80%, (2) 60% ≤ m < 80%, (3) 40% ≤ m < 60%, (4) 20% ≤ m < 40% and (5) m < 20%. Both presence of bark splits and EAB infestation were recorded based on presence/absence: 1 = present, 0 = absent. In addition, we reviewed and extracted data on the same seven variables from the 17 recovered publications that contained detailed data about EAB infestations from 1900 to 2021. All data were used to determine differences between the response variable degree of EAB infestation and the independent variables in the tree host and environmental categories.


Spatiotemporal relationships between ash tree plantings and EAB infestations

To determine the relationship between ash tree plantings and EAB infestations in China, we gathered information on ash tree introductions and plantings from literature sources published in formal databases and other informal reports especially for non-English publications (e.g., local fauna reports) from 1900 to 2021 (Supplementary References). We used the search terms ‘Fraxinus and China’ in Web of Science and ‘tree and introduction and Bai La’ (Bai La: Chinese common name of Fraxinus) in the National Science Database of Forestry (www.lknet.ac.cn/sztsg.htm) to retrieve publications from 1900 to 2021. These searches generated 655 and 105 results, respectively, of which 27 publications (Table S2 in Dang et al. 2021) included details about introduced non-Asian ash trees including ash tree species, planting year, name of province with ash tree plantation, number of these provinces, number of plantings and total area of plantations. Data on five variables were obtained from these 27 publications, including plantings of non-Asian ash trees, planting year, planting provinces, planting times and planting areas. Planting years were divided into eight time periods from 1900 to 2021 (1900–1950 as the first period followed by 10-year periods) and all data on ash tree species, times and areas of plantings were summed for each time period. Data on the distribution of native ash species were obtained from Flora of China (CAS-EBF, 1992). Finally, we mapped the geographical distributions of native and non-Asian ash trees in China. The planting areas of non-Asian ash species, number of provinces with non-Asian ash plantations and numbers of cities with EAB present were summed during each time period from 1900 to 2021 to determine the temporal distribution characteristics of EAB in China.


For complete details see Dang et al. (2021).
Methodology_Citation:
Citation_Information:
Originator: Dang, Yingqiao
Originator: Wei, Ke
Originator: Wang, Xiaoyi
Originator: Duan, Jian J.
Originator: Jennings, David E.
Originator: Poland, Therese M.
Publication_Date: 2021
Title:
Introduced plants induce outbreaks of a native pest and facilitate invasion in the plants' native range: Evidence from the emerald ash borer
Geospatial_Data_Presentation_Form: journal article
Series_Information:
Series_Name: Journal of Ecology
Issue_Identification: 110(3): 595-604
Online_Linkage: https://doi.org/10.1111/1365-2745.13822
Process_Step:
Process_Description:
A catalog entry for this data package was added to the Forest Service Research Data Archive.
Process_Date: 20220929
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Entity_and_Attribute_Information:
Overview_Description:
Entity_and_Attribute_Overview:
The following files are included:

1) "EAB infestation data from 1961 to 2021.xlsx"
This is the original dataset on the EAB infestations obtained from historical publications with field collected data from 1961 to 2021. The explanation of main information of historical occurrences of EAB in China is included in the manuscript and supplementary materials, section "Materials and Methods", "Figure legend", or "Table legend".

2) "Non-Asian ash tree distribution in China.xlsx "
This is the available dataset on the plantings of non-Asian ash trees in China, 1900-2021. The explanation and main results are included in the manuscript and supplementary materials, section "Materials and Methods", "Figure 3", and "Table S2".

3) "Non-Asian ash trees and EAB infestations in North America.xlsx "
This is the original dataset on the non-Asian ash trees and EAB infestations in North America from 1900 to 2021. The explanation and main results are included in the manuscript, section "Materials and Methods" and "Figure 4".

4) "The common garden field study in 2012-2013.xlsx"
This is the original dataset on the species of ash trees infested with EAB at the Institute of Botany, Chinese Academy of Sciences, Beijing, China, 2012-2013. The explanation and main results of the infestations of these trees are included in the manuscript, section "Materials and Methods" and "Table 2".
Entity_and_Attribute_Detail_Citation:
Dang, Yingqiao; Wei, Ke; Wang, Xiaoyi; Duan, Jian J.; Jennings, David E.; Poland, Therese M. 2021. Introduced plants induce outbreaks of a native pest and facilitate invasion in the plants’ native range: Evidence from the emerald ash borer. Journal of Ecology 110(3): 595-604. https://doi.org/10.1111/1365-2745.13822
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Distribution_Information:
Distributor:
Contact_Information:
Contact_Organization_Primary:
Contact_Organization: Dryad: https://datadryad.org/
Resource_Description: 10.5061/dryad.8gtht76qn
Standard_Order_Process:
Digital_Form:
Digital_Transfer_Information:
Format_Name: XLSX
Format_Version_Number: see Format Specification
Format_Specification:
Microsoft Excel Open XML spreadsheet file
File_Decompression_Technique: Files zipped with 7-Zip 19.0
Digital_Transfer_Option:
Online_Option:
Computer_Contact_Information:
Network_Address:
Network_Resource_Name: https://doi.org/10.5061/dryad.8gtht76qn
Fees: None
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Metadata_Reference_Information:
Metadata_Date: 20220928
Metadata_Contact:
Contact_Information:
Contact_Organization_Primary:
Contact_Organization: USDA Forest Service, Northern Research Station
Contact_Person: Therese Poland
Contact_Position: Research Entomologist
Contact_Address:
Address_Type: mailing and physical
Address: 3101 Technology Blvd., Suite F
City: Lansing
State_or_Province: MI
Postal_Code: 48910
Country: USA
Contact_Voice_Telephone: 517-884-8062
Contact_Electronic_Mail_Address: therese.poland@usda.gov
Metadata_Contact:
Contact_Information:
Contact_Organization_Primary:
Contact_Organization: Institute of Forest Ecology, Environment and Protection
Contact_Person: Xiaoyi Wang
Contact_Electronic_Mail_Address: xywang@caf.ac.cn
Metadata_Standard_Name: FGDC Biological Data Profile of the Content Standard for Digital Geospatial Metadata
Metadata_Standard_Version: FGDC-STD-001.1-1999
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