Phenological mismatches mitigate the ecological impact of a biological invader on amphibian communities.

Horizon scans have emerged as a valuable tool to anticipate the incoming invasive alien species (IAS) by judging species on their potential impacts. However, little research has been conducted on quantifying actual impacts and assessing causes of species-specific vulnerabilities to particular IAS due to persistent methodological challenges. The underlying interspecific mechanisms driving species-specific vulnerabilities therefore remain poorly understood, even though they can substantially improve the accuracy of risk assessments. Given that interspecific interactions underlying ecological impacts of IAS are often shaped by phenological synchrony, we tested the hypothesis that temporal mismatches in breeding phenology between native species and IAS can mitigate their ecological impacts. Focusing on the invasive American bullfrog (Lithobates catesbeianus), we combined an environmental DNA (eDNA) quantitative barcoding and metabarcoding survey in Belgium with a global meta-analysis, and integrated citizen-science data on breeding phenology. We examined whether the presence of native amphibian species was negatively related to the presence or abundance of invasive bullfrogs and whether this relationship was affected by their phenological mismatches. The field study revealed a significant negative effect of increasing bullfrog eDNA concentrations on native amphibian species richness and community structure. These observations were shaped by species-specific vulnerabilities to invasive bullfrogs, with late spring- and summer-breeding species being strongly affected, while winter-breeding species remained unaffected. This trend was confirmed by the global meta-analysis. A significant negative relationship was observed between phenological mismatch and the impact of bullfrogs. Specifically, native amphibian species with breeding phenology differing by 6 weeks or less from invasive bullfrogs were more likely to be absent in the presence of bullfrogs than species whose phenology differed by more than 6 weeks with that of bullfrogs. Taken together, we present a novel method based on the combination of aqueous eDNA quantitative barcoding and metabarcoding to quantify the ecological impacts of biological invaders at the community level. We show that phenological mismatches between native and invasive species can be a strong predictor of invasion impact regardless of ecological or methodological context. Therefore, we advocate for the integration of temporal alignment between native and IAS's phenologies into invasion impact frameworks.

Everts T ，Van Driessche C ，Neyrinck S ，Haegeman A ，Ruttink T ，Jacquemyn H ，Brys R ... -  《ECOLOGICAL APPLICATIONS》

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.

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. 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. 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. 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. 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.

Liu X ，Wang S ，Ke Z ，Cheng C ，Wang Y ，Zhang F ，Xu F ，Li X ，Gao X ，Jin C ，Zhu W ，Yan S ，Li Y ... -  《-》

Accurate detection and quantification of seasonal abundance of American bullfrog (Lithobates catesbeianus) using ddPCR eDNA assays.

Everts T ，Halfmaerten D ，Neyrinck S ，De Regge N ，Jacquemyn H ，Brys R ... -  《Scientific Reports》

Bombardier beetles repel invasive bullfrogs.

Invasive non-native predators negatively affect native species; however, some native species can survive the predation pressures of invasive species by using pre-existing antipredator strategies or evolving defenses against invasive predators. The American bullfrog Lithobates catesbeianus (Anura: Ranidae) has been intentionally introduced to many countries and regions, and has impacted native animals through direct predation. Bombardier beetles (Coleoptera: Carabidae: Brachininae: Brachinini) discharge chemicals at a temperature of approximately 100 °C from the tip of the abdomen when they are attacked by predators. This "bombing" can successfully repel predators. However, adults of a native bombardier beetle Pheropsophus (Stenaptinus) occipitalis jessoensis have been reportedly found in the gut contents of the introduced bullfrog L. catesbeianus in Japan. These records suggest that the invasive bullfrog L. catesbeianus attacks the native bombardier beetle P. occipitalis jessoensis under field conditions in Japan; however, the effectiveness of the bombing defense against invasive bullfrogs is unclear. To test the effectiveness of the bombing defense against bullfrogs, we investigated the behavioral responses of L. catesbeianus juveniles to P. occipitalis jessoensis adults under laboratory conditions. Contrary to previous gut content results, almost all the bullfrogs (96.3%) rejected bombardier beetles before swallowing them; 88.9% rejected the beetles after being bombed, and 7.4% stopped attacking the beetles before being bombed. Only 3.7% successfully swallowed and digested the beetle. All of the beetles collected from non-bullfrog-invaded sites could deter bullfrogs, suggesting that the pre-existing defenses of bombardier beetles played an essential role in repelling bullfrogs. When treated beetles that were unable to discharge hot chemicals were provided, 77.8% of bullfrogs successfully swallowed and digested the treated beetles. These results indicate that bombing is important for the successful defense of P. occipitalis jessoensis against invasive bullfrogs. Although invasive bullfrogs have reportedly impacted native insect species, P. occipitalis jessoensis has an existing defense mechanism strong enough to repel the invasive predators.

Sugiura S ，Date T 《PeerJ》

Risk assessment for the native anurans from an alien invasive species, American bullfrogs (Lithobates catesbeianus), in South Korea.

The invasive species are of global concern, and the Invasive American Bullfrog (IAB; Lithobates catesbeianus) is one of the worst invasive amphibian species worldwide. Like other countries, South Korea is also facing challenges from IAB. Although many studies indicated impacts of IAB on native anurans in Korea, the actual risk at the specific level is yet to evaluate. Considering the putative invasiveness of IAB, it is hypothesized that any species with the possibility of physical contact or habitat sharing with them, will have a potential risk. Thus, we estimated and observed their home range, preferred habitats, morphology, behavior, and ecology. Then, comparing with existing knowledge, we assessed risks to the native anurans. We found a home range of 3474.2 ± 5872.5 m2 and identified three types of habitats for IAB. The analyses showed at least 84% of native anurans (frogs and toads) were at moderate to extreme risks, which included all frogs but only 33% of toads. Finally, we recommended immediate actions to conserve the native anurans based on our results. As this study is the first initiative to assess the specific risk level from the invasiveness of L. catesbeianus, it will help the managers to set conservation priorities and strategies.

Park HR ，Rahman MM ，Park SM ，Choi JH ，Kang HJ ，Sung HC ... -  《Scientific Reports》