Habitat connectivity and resident shared predators determine the impact of invasive bullfrogs on native frogs in farm ponds.

Habitat connectivity is considered to have an important role on the persistence of populations in the face of habitat fragmentation, in particular, for species with conservation concern. However, it can also impose indirect negative effects on native species through the spread of invasive species. Here, we investigated direct and indirect effects of habitat connectivity on populations of invasive bullfrogs and native wrinkled frogs and how these effects are modified by the presence of common carp, a resident shared predator, in a farm pond system in Japan. The distribution pattern analysis using a hierarchical Bayesian modelling indicated that bullfrogs had negative effects on wrinkled frogs, and that these negative effects were enhanced with increasing habitat connectivity owing to the metapopulation structure of bullfrogs. The analysis also suggested that common carp mitigated these impacts, presumably owing to a top-down trophic cascade through preferential predation on bullfrog tadpoles. These presumed interspecific interactions were supported by evidence from laboratory experiments, i.e. predation by carp was more intense on bullfrog tadpoles than on wrinkled frog tadpoles owing to the difference in refuge use. Our results indicate that metacommunity perspectives could provide useful insights for establishing effective management strategies of invasive species living in patchy habitats.

Atobe T ，Osada Y ，Takeda H ，Kuroe M ，Miyashita T ... -  《-》

Defenses of whirligig beetles against native and invasive frogs.

Many native insects have evolved defenses against native predators. However, their defenses may not protect them from non-native predators due to a limited shared history. The American bullfrog, Aquarana catesbeiana (Anura: Ranidae), which has been intentionally introduced to many countries, is believed to impact native aquatic animals through direct predation. Adults of whirligig beetles (Coleoptera: Gyrinidae), known for swimming and foraging on the water surface of ponds and streams, reportedly possess chemical defenses against aquatic predators, such as fish. Although whirligig beetles potentially encounter both bullfrogs and other frogs in ponds and lakes, the effectiveness of their defenses against frogs has been rarely studied. To assess whether whirligig beetles can defend against native and non-native frogs, we observed the behavioral responses of the native pond frog, Pelophylax nigromaculatus (Anura: Ranidae), and the invasive non-native bullfrog, A. catesbeiana, to native whirligig beetles, Gyrinus japonicus and Dineutus orientalis, in Japan. Adults of whirligig beetles were provided to frogs under laboratory conditions. Forty percent of G. japonicus and D.orientalis were rejected by P. nigromaculatus, while all whirligig beetles were easily consumed by A. catesbeiana. Chemical and other secondary defenses of G. japonicus and D. orientalis were effective for some individuals of P. nigromaculatus but not for any individuals of A. catesbeiana. These results suggest that native whirligig beetles suffer predation by invasive non-native bullfrogs in local ponds and lakes in Japan.

Sugiura S ，Hayashi M 《PeerJ》

Empirical evidence for effects of invasive American Bullfrogs on occurrence of native amphibians and emerging pathogens.

Invasive species and emerging infectious diseases are two of the greatest threats to biodiversity. American Bullfrogs (Rana [Lithobates] catesbeiana), which have been introduced to many parts of the world, are often linked with declines in native amphibians via predation and the spread of emerging pathogens such as amphibian chytrid fungus (Batrachochytrium dendrobatidis [Bd]) and ranaviruses. Although many studies have investigated the potential role of bullfrogs in the decline of native amphibians, analyses that account for shared habitat affinities and imperfect detection have found limited support for clear effects. Similarly, the role of bullfrogs in shaping the patch-level distribution of pathogens is unclear. We used eDNA methods to sample 233 sites in the southwestern USA and Sonora, Mexico (2016-2018) to estimate how the presence of bullfrogs affects the occurrence of four native amphibians, Bd, and ranaviruses. Based on two-species, dominant-subordinate occupancy models fitted in a Bayesian context, federally threatened Chiricahua Leopard Frogs (Rana chiricahuensis) and Western Tiger Salamanders (Ambystoma mavortium) were eight times (32% vs. 4%) and two times (36% vs. 18%), respectively, less likely to occur at sites where bullfrogs occurred. Evidence for the negative effects of bullfrogs on Lowland Leopard Frogs (Rana yavapaiensis) and Northern Leopard Frogs (Rana pipiens) was less clear, possibly because of smaller numbers of sites where these native species still occurred and because bullfrogs often occur at lower densities in streams, the primary habitat for Lowland Leopard Frogs. At the community level, Bd was most likely to occur where bullfrogs co-occurred with native amphibians, which could increase the risk to native species. Ranaviruses were estimated to occur at 33% of bullfrog-only sites, 10% of sites where bullfrogs and native amphibians co-occurred, and only 3% of sites where only native amphibians occurred. Of the 85 sites where we did not detect any of the five target amphibian species, we also did not detect Bd or ranaviruses; this suggests other hosts do not drive the distribution of these pathogens in our study area. Our results provide landscape-scale evidence that bullfrogs reduce the occurrence of native amphibians and increase the occurrence of pathogens, information that can clarify risks and aid the prioritization of conservation actions.

Hossack BR ，Oja EB ，Owens AK ，Hall D ，Cobos C ，Crawford CL ，Goldberg CS ，Hedwall S ，Howell PE ，Lemos-Espinal JA ，MacVean SK ，McCaffery M ，Mosley C ，Muths E ，Sigafus BH ，Sredl MJ ，Rorabaugh JC ... -  《ECOLOGICAL APPLICATIONS》

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》

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 ... -  《-》