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. 全球化时代下，物种引入速率不断加快，同域共存的外来物种愈发常见。阐明多种入侵生物的复合生态效应，不仅对于试图缓解生物多样性丧失的野生动物管理者而言至关重要，同时也能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，学界对多种同域入侵物种的影响仍知之甚少。
2. 美洲牛蛙（Lithobates catesbeianus = Rana catesbeiana）与红沼泽螯虾（Procambarus clarkii）是全球诸多区域广泛分布的两种水生入侵物种。二者可与本土无尾类动物共存于各类永久性静水水体中，为探究不同营养级的多种入侵生物对本土物种的复合效应提供了理想的模式系统。
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，以及中国舟山群岛157处水体的十年野外调查数据，发现当两种入侵生物共存时，在螯虾密度较高的生境中，牛蛙对本土无尾类的影响会被削弱。
4. 全球食性分析结果显示，无论在本土还是入侵牛蛙种群中，螯虾的存在都会降低牛蛙捕食的本土无尾类猎物数量。在校正了不同水体、岛屿与调查时段间观测存在的伪重复问题后，基于广义线性混合模型（generalized linear mixed models, GLMMs）的模型平均分析表明：仅针对入侵牛蛙的野外观测，以及螯虾密度较低的共同入侵生境观测中，牛蛙密度与本土无尾类种群密度呈负相关关系。但当两种入侵生物在高螯虾密度生境中共存时，这一负相关关系不复存在。结构方程模型（structural equation modeling, SEM）分析进一步证实，螯虾与牛蛙间的负相互作用可缓解牛蛙对本土蛙类的影响。
5. 本研究结果为不同营养级的两种同域入侵物种对本土物种产生的密度依赖性拮抗效应提供了全新证据。本研究强调，在制定优先保护与管理措施时，需考虑共同入侵物种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。