Native predators living in invaded areas: responses of terrestrial amphibian species to an Argentine ant invasion

Predator–prey interactions play a key role in the success and impacts of invasive species. However, the effects of invasive preys on native predators have been poorly studied. Here, we first reviewed hypotheses describing potential relationships between native predators and invasive preys. Second, we examined how an invasive prey, the Argentine ant (Linepithema humile), affected a native terrestrial amphibian community. In the field, we looked at the structure of the amphibian community in invaded versus uninvaded areas and characterized amphibian trophic ecology. The amphibian community sampled seemed to show a species-dependent response in abundance to invasion: adults of the natterjack toad (Bufo calamita), the species demonstrating the highest degree of ant specialization, were less abundant in invaded areas. Although available ant biomass was significantly greater in invaded than in uninvaded areas (only Argentine ants occurred in the former), amphibians consumed relatively fewer ants in invaded areas. In the lab, we quantified amphibian consumption of Argentine ants versus native ants and assessed whether consumption patterns could have been influenced by prior exposure to the invader. The lab experiments corroborated the field results: amphibians preferred native ants over Argentine ants, and prior exposure did not influence consumption. Differences in preference explained why amphibians consumed fewer Argentine ants in spite of their greater relative availability; they might also explain why the most ant-specialized amphibians seemed to avoid invaded areas. Our results suggest the importance to account for predator feeding capacities and dietary ranges to understand the effects of invasive species at higher trophic levels.     

Native range climate is insufficient to predict anuran invasive potential

Niche conservatism explains biological invasions worldwide. However, a plethora of ecological processes may lead invasive species to occupy environments that are different from those found within native ranges. Here, we assess the potential invadable areas of  the world’s most pervasive invasive amphibians: the cane toad, Rhinella marina?+?R. horribilis, and the North American bullfrog, Lithobates catesbeianus. The uncontrolled spread of such voracious, large-bodied, and disease-tolerant anurans has been documented to impact native faunas worldwide. To disentangle their invasion-related niche dynamics, we compared the predictive ability and distributional forecasts of ecological niche models calibrated with information from native, invaded and pooled (native?+?invaded) ranges. We found that including occurrences from invaded ranges improved model accuracy for both studied species. Non-native occurrences also accounted for 54% and 61% increase in the total area of potential distribution of the cane toad and bullfrog, respectively. Besides, the latter species occupied locations with climatic conditions that are more extreme than those found within its native range. Our results indicate that the occupancy of environments different from those found in native ranges increases the overall potential distribution of the studied invasive anuran species. Therefore, climate information on native ranges alone is insufficient to explain and anticipate the distributional patterns of invasion of cane toads and bullfrogs, underestimating predictions of potential invadable distribution. Moreover, such an observed expansion of realized niches towards occupancy of climates not found within native ranges also has clear implications for invasion risk assessments based on climate modelling worldwide.

     

Let’s eat out,there’s crayfish for dinner: American bullfrog niche shifts inside and outside native ranges and the effect of introduced crayfish

In invasion ecology, niche width has been recognized as a crucial factor for the outcome of an invasion. A common characteristic of successful invaders seems to be a broad niche width, and their impact on native communities may increase with increasing niche size. Overall, successful invader predators are predicted to shift their niche width by broadening it from native to invaded conditions. The scarcity of ecological studies examining invasive species in their native ranges prevents researchers from knowing if the prevalence of generalist invaders represents conservatism of broad native-range niches or instead niche shifts as a result of different processes acting in the invaded areas. Here we reviewed literature on trophic niche of the predatory invader American bullfrog (Lithobates catesbeianus) in both native and invaded ranges. We used statistical and graphic tools to analyse possible shifts in dietary niche width and the effect of introduced crayfish on the feeding strategy of L. catesbeianus. Globally, our results indicate that food sources used by the species differed in native and invaded sites, with a narrower trophic niche width in invaded areas. However, this pattern was disrupted by the occurrence of introduced crayfish that represents the major driver of the observed niche-width variation. Our data shed light on possible complications in interpreting and predicting patterns of biological invasions due to the interaction among species from different trophic levels that apparently disrupt general patterns that are likely bound to be idiosyncratic and complex.     

Plant community composition and structural characteristics of an invaded forest in the Galápagos

Non-native species have invaded habitats worldwide, greatly impacting the structure and function of native communities and ecosystems. To better understand mechanisms of invasion impacts and how to restore highly impacted and transformed ecosystems, studies are needed that evaluate invader effects on both biotic communities and structural characteristics. On Santa Cruz Island in Galápagos we compared biotic (plant species richness, diversity, and community composition) and structural (canopy openness, forest height, and leaf litter) characteristics of a relic forest dominated by an endemic and highly threatened tree and a forest dominated by an invasive tree. The forests are located within the historical distribution of the endemic tree, which now occupies only 1% of its original extent. We found that the invaded forest had 42% lower native plant species richness and 17% less plant diversity than the endemic tree dominated forest. Additionally, with the invader there was 36% greater non-native plant species richness, 37% higher non-native plant diversity, and highly dissimilar plant composition when compared to the endemic-dominated forest. Additionally, the invaded forest had a more open and taller tree canopy and greater leaf litter cover than native forest. The presence of the invasive tree and the associated forest structural changes were the primary factors in models that best explained higher non-native diversity in the invaded forest. Our correlational results suggest that an invasive tree has significantly altered plant assemblage and forest structural characteristics in this unique ecosystem. Experiments that remove the invader and evaluate native plant community responses are needed to identify thresholds for practical restoration of this threatened and biologically unique native forest.     

Invasive ants as back-seat drivers of native ant diversity decline in New Caledonia

Biological invasions are typically associated with disturbance, which often makes their impact on biodiversity unclear—biodiversity decline might be driven by disturbance, with the invader just being a ‘passenger’. Alternatively, an invader may act as a ‘back-seat driver’, being facilitated by disturbance that has already caused some biodiversity decline, but then causing further decline. Here we examine the interactive effects of anthropogenic fire and invasive ant species (Anoplolepis gracilipes or Wasmannia auropunctata) on native ant diversity in New Caledonia, a globally recognized biodiversity hotspot. We first examined native ant diversity at nine paired burnt and unburnt sites, with four pairs invaded by Anoplolepis, 5 years after an extensive fire. In the absence of invasion, native epigaeic ants were resilient to fire, but native ant richness and the abundance of Forest Opportunists were markedly lower in invaded burnt sites. Second, we examined native ant diversity along successional gradients from human-derived savanna to natural rainforest in the long-term absence of fire, where there was a disconnection between disturbance-mediated variation in microhabitat and the abundance of the disturbance specialist Wasmannia. All native ant diversity responses (total abundance, richness, species composition, functional group richness and the abundance of Forest Opportunists) declined independently of microhabitat variables but in direct association with high Wasmannia abundance. Our results indicate that invasive ants are acting as back-seat drivers of biodiversity decline in New Caledonia, with invasion facilitated by disturbance but then causing further biodiversity decline.     

Current status of alien vertebrates in the Galápagos Islands: invasion history, distribution, and potential impacts

Human activity has promoted the invasion of the Galápagos Islands by alien species from each of the five classes of vertebrates. We review the current distribution of alien vertebrates in the archipelago, their impacts on native species, and management efforts aimed at alien vertebrates. A total of 44 species have been reported in the archipelago, with 20 species establishing feral populations. Mammals were the first group arriving in the archipelago and remain the most numerous, with 10 established species. Alien birds invaded after mammals and four species have established populations. Reptiles, amphibians, and fish invaded later and are represented by three, one, and two species, respectively. Alien mammals are the most injurious to native biota, contributing to the decline or extinction of several species. Aside from mammals, no other class of alien vertebrate has had documented impacts on native species. Several populations of large and medium-sized mammals and birds have been eradicated.     

First Evidence of <Emphasis Type="Italic">Batrachochytrium dendrobatidis</Emphasis> in China: Discovery of Chytridiomycosis in Introduced American Bullfrogs and Native Amphibians in the Yunnan Province,China

Although the chytrid fungus Batrachochytrium dendrobatidis (Bd), the etiological agent of amphibian chytridiomycosis, has been implicated in mass mortality and population declines on several continents around the world, there have been no reports on the presence of Bd infections in amphibians in China. We employed quantitative PCR and histological techniques to investigate the presence of Bd in introduced North American bullfrogs (Rana catesbeiana) (referred to hereafter as bullfrog) and native amphibians in bullfrog-invaded areas of the Yunnan Province, China. A total of 259 samples at five wild sites were collected between June and September in 2007 and 2008, including bullfrogs and four native amphibian species (Rana pleuraden, Rana chaochiaoensis, Odorrana andersonii, and Bombina maxima). In addition, 37 samples of adult bullfrogs were obtained from a food market. Bd infections were discovered in bullfrogs and three native amphibian species from all of the surveyed sites. Of the 39 Bd-positive samples, 35 were from wild-caught bullfrog tadpoles, postmetamorphic bullfrogs, R. pleuraden, R. chaochiaoensis, and O. andersonii, and four were from adult bullfrogs from the market. Our results provide the first evidence of the presence of Bd in Chinese amphibians, suggesting that native amphibian diversity in China is at risk from Bd. There is an urgent need to monitor the distribution of Bd in amphibians in China and understand the susceptibility of native amphibian species to chytridiomycosis. Strict regulations on the transportation of bullfrogs and the breeding of bullfrogs in markets and farms should be drafted in order to stop the spread of Bd by bullfrogs.     

Population genetics reveals origin and number of founders in a biological invasion

Propagule pressure is considered the main determinant of success of biological invasions: when a large number of individuals are introduced into an area, the species is more likely to establish and become invasive. Nevertheless, precise data on propagule pressure exist only for a small sample of invasive species, usually voluntarily introduced. We studied the invasion of the American bullfrog, Rana catesbeiana, into Europe, a species that is considered a major cause of decline for native amphibians. For this major invader with scarce historical data, we used population genetics data (a partial sequence of the mitochondrial cytochrome b gene) to infer the invasion history and to estimate the number of founders of non-native populations. Based on differences between populations, at least six independent introductions from the native range occurred in Europe, followed by secondary translocations. Genetic diversity was strongly reduced in non-native populations, indicating a very strong bottleneck during colonization. We used simulations to estimate the precise number of founders and found that most non-native populations derive from less than six females. This capability of invasion from a very small number of propagules challenges usual management strategies; species with such ability should be identified at an early stage of introduction.     

Invasive cane toads are unique in shape but overlap in ecological niche compared to Australian native frogs

Invasive species are an important issue worldwide but predicting invasiveness, and the underlying mechanisms that cause it, is difficult. There are several primary hypotheses to explain invasion success. Two main hypothesis based on niche spaces stand out as alternative, although not exclusive. The empty niche hypothesis states that invaders occupy a vacant niche space in the recipient community, and the niche competition hypothesis states that invaders overlap with native species in niche space. Studies on trait similarity/dissimilarity between the invader and native species can provide information on their niche overlap. Here, we use the highly invasive and well‐studied cane toad (Rhinella marina) to test these two hypotheses in Australia, and assess its degree of overlap with native species in several niche dimensions. We compare extensive morphological and environmental data of this successful invader to 235 species (97%) of native Australian frogs. Our study is the first to document the significant morphological differences between the invasive cane toad and a continent‐wide frog radiation: despite significant environmental overlap, cane toads were distinct in body size and shape from most Australian frog species, suggesting that in addition to their previously documented phenotypic plasticity and wide environmental and trophic niche breadth, their unique shape also may have contributed to their success as an invasive species in Australia. Thus, the invasive success of cane toads in Australia may be explained through them successfully colonizing an empty niche among Australian anurans. Our results support that the cane toad's distinct morphology may have played a unique role in the invasiveness of this species in Australia, which coupled with a broad environmental niche breadth, would have boosted their ability to expand their distribution across Australia. We also propose RLLR (Relative limb length ratio) as a potentially useful measure of identifying morphological niche uniqueness and a potential measure of invasiveness potential in anuran amphibians.     

Invasion of the acoustic niche: variable responses by native species to invasive American bullfrog calls

Biological invasions are a major threat to biodiversity. Invasive species that use acoustic communication can affect native species through interference in the acoustic niche. The American Bullfrog Lithobates catesbeianus is a highly invasive anuran that is widely distributed in the Brazilian Atlantic Rainforest. Adult male bullfrogs emit loud advertisement calls at frequencies that overlap with the calls of several native species of frogs. Given that spectral overlap is a major factor in acoustic masking, the purpose of this study was to test the effects of the acoustic invasion of L. catesbeianus on native frogs that have calls with and without spectral overlap with the invader. In field experiments, we exposed calling males of two overlapping species and two non-overlapping species to recorded bullfrog vocalizations, white noise, and the vocalization of another native frog species. To identify effects, we compared calls recorded before, during, and after exposure. Our results showed that native species altered their calls in response to the bullfrog calls. However, we also observed similar responses to white noise and heterospecific native calls. Both the invasive and heterospecific calls were emitted at low frequencies, which suggests that the observed responses might be specific to low-frequency calls. Our results provide evidence that the introduction of new sounds can cause native species to modify their calls, and that responses to exogenous sounds are species- and stimulus-specific.     

浙江东部牛蛙的自然种群及潜在危害

牛蛙(Rana catesbeiana)的入侵已成为一些本地两栖类种群数量下降或灭绝的主要因素之一。1959年牛蛙被引入中国大陆,但直到1990年才开始在国内大范围饲养。牛蛙的自然种群在国内一直未见报道。我们于2003年9—11月调查了浙江省东部5区3县的牛蛙种群,发现在岱山、秀山、六横及佛渡岛上有牛蛙分布,共捕获23只牛蛙,包括4只成年个体,18个亚成体和1只蝌蚪。于2004年1月和2月在岱山捕获28只蝌蚪。结果显示：(1)牛蛙的蝌蚪能在当地越冬成活,说明牛蛙在上述4岛成功地建立了自然种群;(2)牛蛙主要分布于水库、池塘和溪流,牛蛙的生境与6种当地蛙有部分重叠;(3)养殖时管理不善造成的牛蛙逃逸,以及牛蛙价格过低而导致养殖户将牛蛙弃置野外可能是牛蛙入侵的主要原因。牛蛙对当地蛙的潜在威胁很大,开展牛蛙的分布、食性和种群动态研究是当务之急。     

Using molecular diet analysis to inform invasive species management: A case study of introduced rats consuming endemic New Zealand frogs

The decline of amphibians has been of international concern for more than two decades, and the global spread of introduced fauna is a major factor in this decline. Conservation management decisions to implement control of introduced fauna are often based on diet studies. One of the most common metrics to report in diet studies is Frequency of Occurrence (FO), but this can be difficult to interpret, as it does not include a temporal perspective. Here, we examine the potential for FO data derived from molecular diet analysis to inform invasive species management, using invasive ship rats (Rattus rattus) and endemic frogs (Leiopelma spp.) in New Zealand as a case study. Only two endemic frog species persist on the mainland. One of these, Leiopelma archeyi, is Critically Endangered (IUCN 2017) and ranked as the world's most evolutionarily distinct and globally endangered amphibian (EDGE, 2018). Ship rat stomach contents were collected by kill‐trapping and subjected to three methods of diet analysis (one morphological and two DNA‐based). A new primer pair was developed targeting all anuran species that exhibits good coverage, high taxonomic resolution, and reasonable specificity. Incorporating a temporal parameter allowed us to calculate the minimum number of ingestion events per rat per night, providing a more intuitive metric than the more commonly reported FO. We are not aware of other DNA‐based diet studies that have incorporated a temporal parameter into FO data. The usefulness of such a metric will depend on the study system, in particular the feeding ecology of the predator. Ship rats are consuming both species of native frogs present on mainland New Zealand, and this study provides the first detections of remains of these species in mammalian stomach contents.     

Antipredator Behavioral Responses of Native and Exotic Tadpoles to Novel Predator

Factors related to the invasion process, such as high abundance of invaders, residence time, and functional distinctiveness, are well documented, but less attention has been given to the effects of antipredator strategy of invasive species during colonization. In this study, we explored the antipredator strategy of an introduced species by comparing the predator avoidance behaviors of two native anuran species and one introduced("exotic") species in the presence of different predators. The two native anuran species used in the study were Black-spotted Pond Frog Rana nigromaculata and Terrestrial Frog Rana limnocharis. The introduced(invasive) species used was American bullfrog Lithobates catesbeianus. Chinese pond turtle Chinemys reevesii, Red-backed rat snake Elaphe rufodorsata, and Big-headed turtle Platysternon megacephalum were used as predator species. Chinese pond turtles and Red-backed rat snakes are native predators of Black-spotted Pond Frogs and Terrestrial Frogs, while Big-headed turtles are novel("unfamiliar") to the two frogs. All three predator species are novel("unfamiliar") to the American bullfrog. The results show that tadpoles of the two native species displayed behaviors of recognizing the two native predators, but did not display the capability of identifying the novel predator. Results from our study also suggest that American bullfrog tadpoles exhibited strong antipredator behavioral responses by displaying the capability of identifying "unfamiliar" predators without cohabitation history and prior exposure to them. Such antipredator behavioral responses could have resulted in more favorable outcomes for an invading species during the invasive introductory process.     

Invasive North American bullfrogs transmit lethal fungus <Emphasis Type="Italic">Batrachochytrium dendrobatidis</Emphasis> infections to native amphibian host species

Invasive species can be a threat to native species in several ways, including transmitting lethal infections caused by the parasites they carry. However, invasive species may also be plagued by novel and lethal infections they acquire when invading, making inferences regarding the ability of an invasive host to vector disease difficult from field observations of infection and disease. This is the case for the pathogenic fungus Batrachochytrium dendrobatidis (Bd) in Europe and one invasive host species, the North American bullfrog Lithobates catesbeianus, hypothesized to be responsible for vectoring lethal infection to European native amphibians. We tested this hypothesis experimentally using the alpine newt Ichthyosaura alpestris as our model native host. Our results show that infected bullfrog tadpoles are effective vectors of Bd. Native adult newts co-housed with experimentally infected bullfrog tadpoles became Bd infected (molecular and histological tests). Moreover, the exposed adult newts suffered mortality while the majority of infected bullfrog tadpoles survived until metamorphosis. These results cannot resolve the historical role of alien species in establishing the distribution of Bd across Europe or other regions in the world where this species was introduced, but they show its potential role as a Bd reservoir capable of transmitting lethal infections to native amphibians. Finally, our results also suggest that the removal of infected bullfrogs from aquatic environments may serve to reduce the availability of Bd in European amphibian communities, offering another justification for bullfrog eradication programmes that are currently underway or may be considered.     

Invasive plant suppresses the growth of native tree seedlings by disrupting belowground mutualisms

The impact of exotic species on native organisms is widely acknowledged, but poorly understood. Very few studies have empirically investigated how invading plants may alter delicate ecological interactions among resident species in the invaded range. We present novel evidence that antifungal phytochemistry of the invasive plant, Alliaria petiolata, a European invader of North American forests, suppresses native plant growth by disrupting mutualistic associations between native canopy tree seedlings and belowground arbuscular mycorrhizal fungi. Our results elucidate an indirect mechanism by which invasive plants can impact native flora, and may help explain how this plant successfully invades relatively undisturbed forest habitat.     

Integrative Study of Brazilian Anurans: Geographic Distribution,Size, Environment,Taxonomy, and Conservation

Most megadiversity regions lack basic wild animal diversity information such as species lists. This absence of basic knowledge restricts the development and effectiveness of conservation action plans, which are urgently needed for animal groups such as amphibians, the most threatened vertebrate group in the world. In this study, we estimated Brazilian anuran diversity based on species range distribution shapes and evaluated factors that likely affect species lists, such as current taxonomy knowledge, current number of specimens collected in each region, biome characteristics, and anuran size (snout–vent length). We were able to demonstrate differences among the distributional patterns of species within each biome and each Brazilian federative state and among certain factors that influence their diversity, such as latitudinal variation. In this integrative study, we provide zoogeographic information about the richest (in terms of anuran biodiversity) country in the world (at least 849 described species, about 60% of which are endemic), which may be fundamental to future conservation actions in Brazil.     

Scaling the consequences of interactions between invaders from the individual to the population level

The impact of human‐induced stressors, such as invasive species, is often measured at the organismal level, but is much less commonly scaled up to the population level. Interactions with invasive species represent an increasingly common source of stressor in many habitats. However, due to the increasing abundance of invasive species around the globe, invasive species now commonly cause stresses not only for native species in invaded areas, but also for other invasive species. I examine the European green crab Carcinus maenas, an invasive species along the northeast coast of North America, which is known to be negatively impacted in this invaded region by interactions with the invasive Asian shore crab Hemigrapsus sanguineus. Asian shore crabs are known to negatively impact green crabs via two mechanisms: by directly preying on green crab juveniles and by indirectly reducing green crab fecundity via interference (and potentially exploitative) competition that alters green crab diets. I used life‐table analyses to scale these two mechanistic stressors up to the population level in order to examine their relative impacts on green crab populations. I demonstrate that lost fecundity has larger impacts on per capita population growth rates, but that both predation and lost fecundity are capable of reducing population growth sufficiently to produce the declines in green crab populations that have been observed in areas where these two species overlap. By scaling up the impacts of one invader on a second invader, I have demonstrated that multiple documented interactions between these species are capable of having population‐level impacts and that both may be contributing to the decline of European green crabs in their invaded range on the east coast of North America.     

Do a threatened native amphibian and its invasive congener differ in response to human alteration of the landscape?

Anthropogenic changes to habitat are a global phenomenon and the impact of these changes may act in tandem to cause loss of biodiversity. One major global change is the introduction of invasive species. In order to determine whether other human impacts might correlate with populations of invaders, we examined the habitat correlates of distribution, persistence and reproduction of a global invader, the American bullfrog (Rana catesbeiana). We then compared these correlates with those of a threatened, native congener, the California red-legged frog (Rana draytonii). We found striking differences between the two species in response to habitat fragmentation and degradation. Our work suggests that human alteration of habitat, in particular the hydrology of freshwater sites and through building roads, favors this invasive species across the landscape.     

The invasive bullfrog <Emphasis Type="Italic">Lithobates catesbeianus</Emphasis> in oases of Baja California Sur,Mexico: potential effects in a fragile ecosystem

The American bullfrog (Lithobates catesbeianus), considered as one of the world’s worst invasive species because of its negative effects on native fauna, has been introduced into over 40 countries in four continents. The invasion status in Mexico is poorly known. The first known record for this species in the Peninsula of Baja California, northwestern Mexico is an individual collected 35 years ago. A great portion of the peninsula is an arid desert where the sources of freshwater are the spring-fed oasis and mountain arroyos that support rare and endemic species closely associated with wetland conditions. Humans, who have introduced alien species, inhabit many of those oases. The aim of this work was to document the presence of the exotic bullfrog in 40 oases and mountain arroyos in Baja California Sur state during 2006–2009. Bullfrogs were found in 25% of the oases sampled; 15% have confirmed records of breeding populations and five oases are new location records. Our results show a considerable increase (50%) in the number of oasis invaded by bullfrogs in only 8 years. The animal populations of rare or endemic species associated with oases would be threatened by the arrival of bullfrogs. Actions for their control and eradication are urgently needed.     

Low resource availability limits weed invasion of tropical savannas

The savanna biome is one of the least invaded among global biomes, although the mechanisms underpinning its resistance to alien species relative to other biomes is not well understood. Invaders generally are at the resource acquisitive end of functional global plant trait variation and in low-resource savanna environments we might expect that successful invaders will only outperform native species under resource rich or highly disturbed conditions. However, invaders may also directly exploit resource stressed environments using resource conservative traits in some situations. It’s also possible that successful invaders and native species largely overlap in their trait profiles indicating site specific environmental factors are responsible for invader success in particular contexts rather than a general trait and functional divergence between invaders and native species. To address these various hypotheses, we compared a suite of morphological and physiological traits in graminoid and herbaceous native and co-occurring invasive plant species across a range of habitats in savannas of the Kimberley region of northern Australia. Invader grass species had traits associated with resource acquisition and fast growth rates, such as high SLA and leaf nutrient contents. In contrast, dominant native perennial grasses had traits characteristic of resource conservation and slow growth in resource stressed conditions. Trait profiles among invasive forbs and legumes exhibited stress tolerant traits relative to their native counterparts. Invaders also displayed strong divergence in reproductive traits, suggesting diverse responses to disturbance not indicated by leaf economic traits alone. These results suggest that savannas may be resistant to invaders with resource acquisitive traits due to their strong resource limitation.