Data from: More invaders do not result in heavier impacts: the effects of nonnative bullfrogs on native anurans are mitigated by high densities of nonnative crayfish

1.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
co-exist 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 generalized linear
mixed models (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 modeling (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.

1. 随着全球化时代物种引入速率不断加快，共存的外来入侵物种愈发普遍。阐明多种入侵生物的综合生态影响，不仅对致力于缓解生物多样性丧失的野生动物管理者至关重要，同时也为解析自然生态系统中入侵成功机制与物种共存机理提供了关键视角。相较于针对单一入侵物种影响的大量研究关注，学界对多种共存入侵物种的影响却知之甚少。
2. 美洲牛蛙（Lithobates catesbeianus = Rana catesbeiana）与红沼泽螯虾（Procambarus clarkii）是全球多个区域广泛分布的水生入侵物种。它们与本土无尾类动物共存于各类永久性静水环境中，为探究不同营养级的多重入侵者对本土物种的联合效应提供了理想的模型系统。
3. 本研究依托覆盖34个本土与入侵牛蛙种群的全球食性分析数据，以及中国舟山群岛157个水体的10年野外监测数据，发现当两种入侵者共存时，高螯虾密度会削弱牛蛙对本土无尾类的影响。
4. 全球食性分析结果显示，无论牛蛙处于本土种群还是入侵种群，螯虾的存在均会减少其捕食的本土无尾类猎物数量。在校正不同水体、岛屿与调查时段间的伪重复问题后，基于广义线性混合模型（generalized linear mixed models, GLMMs）的模型平均分析表明：仅存在入侵牛蛙的野外观测，以及螯虾密度较低的共入侵观测中，牛蛙密度与本土无尾类种群密度呈负相关关系；但当两种入侵者以高密度共存时，这一负相关关系消失。结构方程模型（structural equation modeling, SEM）分析进一步验证，螯虾与牛蛙间的负向相互作用，可缓解牛蛙对本土蛙类的负面影响。
5. 本研究结果为不同营养级的两种同域入侵者对本土物种产生的密度依赖性拮抗效应提供了新证。本研究强调，在制定保护与管理优先级策略时，需考虑共入侵者与本土物种间的复杂相互作用，这将助力构建更为精准的入侵影响预测框架。