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More invaders do not result in heavier impacts: The effects of non-native bullfrogs on native anurans are mitigated by high densities of non-native crayfish
Liu, Xuan1; Wang, Supen1; Ke, Zunwei1,2,3; Cheng, Chaoyuan1,2; Wang, Yihua1,2; Zhang, Fang1,2,4; Xu, Feng1,2,5; Li, Xianping1,2; Gao, Xu1,2; Jin, Changnan1,2,6; Zhu, Wei1,2; Yan, Shaofei1,2,7; Li, Yiming1
2018-05-01
Source PublicationJOURNAL OF ANIMAL ECOLOGY
ISSN0021-8790
Volume87Issue:3Pages:850-862
Corresponding AuthorLiu, Xuan(liuxuan@ioz.ac.cn) ; Li, Yiming(liym@ioz.ac.cn)
Abstract1. With accelerating species introductions in an era of globalization, co-occurring alien species have become increasingly common. Understanding the combined ecological impacts of multiple invaders is not only crucial for wildlife managers attempting to ameliorate biodiversity loss, but also provides key insights into invasion success and species coexistence mechanisms in natural ecosystems. Compared with much attentions given to single-invader impacts, little is known about the impacts of multiple co-occurring invaders. 2. The American bullfrog (Lithobates catesbeianus = Rana catesbeiana) and the red swamp crayfish (Procambarus clarkii) are two aquatic invasive species in many different areas of the globe. They coexist with native anurans in a variety of permanent lentic waters, which provide an ideal model system to explore the combined effects of multiple invaders from different trophic levels on native species. 3. Based on a global diet analysis covering 34 native and invasive bullfrog populations, and data from 10-year field surveys across 157 water bodies in the Zhoushan Archipelago, China, we observed a reduced impact of bullfrogs on native anurans at high crayfish densities when the two invaders co-occurred. 4. The global diet analysis showed that crayfish occurrence reduced the number of native anuran prey consumed by bullfrogs in both native and invasive populations. After accounting for pseudoreplication of different observations among water bodies, islands, and survey time, model averaging analyses based on GLMMs showed a negative relationship between bullfrog density and native anuran densities for field observations of invasive bullfrogs alone and co-invaded observations with low crayfish density. However, this negative relationship disappeared when the two invaders co-occurred with high crayfish density. Structural equation modelling (SEM) analyses further validated that the impacts of bullfrogs on native frogs were mitigated by the negative interactions between crayfish and bullfrogs. 5. Our results provide novel evidence of a density-dependent antagonistic effect of two sympatric invaders from different trophic levels on native species. This study highlights the importance of considering complex interactions among co-invaders and native species when prioritizing conservation and management actions and will facilitate the development of a more precise framework to predict invasion impacts.
Keywordamphibian decline biological invasions impact predation species interaction
DOI10.1111/1365-2656.12793
WOS KeywordINVASIVE SPECIES REMOVAL ; PROCAMBARUS-CLARKII ; RANA-CATESBEIANA ; LITHOBATES-CATESBEIANUS ; INTRODUCED CRAYFISH ; BATRACHOCHYTRIUM-SALAMANDRIVORANS ; BIOLOGICAL INVASIONS ; IBERIAN AMPHIBIANS ; DAISHAN ISLAND ; GLOBAL DECLINE
Indexed BySCI
Language英语
Funding ProjectNational Natural Science Foundation of China[31530088] ; National Natural Science Foundation of China[31572284] ; Youth Innovation Promotion Association of Chinese Academy of Sciences[2015066] ; Chinese Academy of Sciences[KFZD-SW-208-09]
Funding OrganizationNational Natural Science Foundation of China ; Youth Innovation Promotion Association of Chinese Academy of Sciences ; Chinese Academy of Sciences
WOS Research AreaEnvironmental Sciences & Ecology ; Zoology
WOS SubjectEcology ; Zoology
WOS IDWOS:000430059900028
PublisherWILEY
Citation statistics
Cited Times:7[WOS]   [WOS Record]     [Related Records in WOS]
Document Type期刊论文
Identifierhttp://ir.igsnrr.ac.cn/handle/311030/57389
Collection中国科学院地理科学与资源研究所
Corresponding AuthorLiu, Xuan; Li, Yiming
Affiliation1.Chinese Acad Sci, Inst Zool, Key Lab Anim Ecol & Conservat Biol, Beijing, Peoples R China
2.Univ Chinese Acad Sci, Beijing, Peoples R China
3.Hanjiang Normal Univ, Dept Biol Chem & Environm Engn, Shiyan, Peoples R China
4.Anhui Normal Univ, Coll Life Sci, Wuhu, Peoples R China
5.Chinese Acad Sci, Xinjiang Inst Ecol & Geog, Key Lab Biogeog & Bioresources Arid Land, Urumqi, Peoples R China
6.Chinese Acad Sci, Inst Geog Sci & Nat Resources Res, Chinese Natl Geog, Beijing, Peoples R China
7.Anhui Univ, Sch Resources & Environm Engn, Hefei, Anhui, Peoples R China
Recommended Citation
GB/T 7714
Liu, Xuan,Wang, Supen,Ke, Zunwei,et al. More invaders do not result in heavier impacts: The effects of non-native bullfrogs on native anurans are mitigated by high densities of non-native crayfish[J]. JOURNAL OF ANIMAL ECOLOGY,2018,87(3):850-862.
APA Liu, Xuan.,Wang, Supen.,Ke, Zunwei.,Cheng, Chaoyuan.,Wang, Yihua.,...&Li, Yiming.(2018).More invaders do not result in heavier impacts: The effects of non-native bullfrogs on native anurans are mitigated by high densities of non-native crayfish.JOURNAL OF ANIMAL ECOLOGY,87(3),850-862.
MLA Liu, Xuan,et al."More invaders do not result in heavier impacts: The effects of non-native bullfrogs on native anurans are mitigated by high densities of non-native crayfish".JOURNAL OF ANIMAL ECOLOGY 87.3(2018):850-862.
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