A native apex predator limits an invasive mesopredator and protects native prey: Tasmanian devils protecting bandicoots from cats

Apex predators can limit the abundance and behaviour of mesopredators, thereby reducing predation on smaller species. We know less about whether native apex predators are effective in suppressing invasive mesopredators, a major global driver of vertebrate extinctions. We use the severe disease‐induced decline of an apex predator, the Tasmanian devil, as a natural experiment to test whether devils limit abundance of invasive feral cats and in turn protect smaller native prey. Cat abundance was c. 58% higher where devils had declined, which in turn negatively affected a smaller native prey species. Devils had a stronger limiting effect on cats than on a native mesopredator, suggesting apex predators may have stronger suppressive effects on evolutionarily naive species than coevolved species. Our results highlight how disease in one species can affect the broader ecosystem. We show that apex predators not only regulate native species but can also confer resistance to the impacts of invasive populations. Apex predators could therefore be a powerful but underutilised tool to prevent biodiversity loss.     

Do native predators benefit from non‐native prey?

Despite knowledge on invasive species’ predatory effects, we know little of their influence as prey. Non‐native prey should have a neutral to positive effect on native predators by supplementing the prey base. However, if non‐native prey displace native prey, then an invader's net influence should depend on both its abundance and value relative to native prey. We conducted a meta‐analysis to quantify the effect of non‐native prey on native predator populations. Relative to native prey, non‐native prey similarly or negatively affect native predators, but only when studies employed a substitutive design that examined the effects of each prey species in isolation from other prey. When native predators had access to non‐native and native prey simultaneously, predator abundance increased significantly relative to pre‐invasion abundance. Although non‐native prey may have a lower per capita value than native prey, they seem to benefit native predators by serving as a supplemental prey resource.     

Alien Invasions and the Game of Hide and Seek in Patagonia

The introduction, establishment and spread of alien species is a major threat to biodiversity and the provision of ecosystem services for human wellbeing. In order to reduce further loss of biodiversity and maintain productive and sustainable ecosystems, understanding the ecological mechanisms underlying species invasions and avoiding potentially harmful effects on native communities is urgently needed, but largely lacking. We here demonstrate, by means of hydroacoustics and advanced spatial modelling, how native fish species as a result of previous exposure to native predators may successfully respond to invasive novel predators through a complicated game of hide and seek, minimizing spatio-temporal overlap with predators, and potentially facilitating coexistence between native prey species (Galaxiids) and introduced novel predators (Salmonids) in a deep Andean lake, Patagonia.     

Complex impact of an invasive crayfish on freshwater food webs

Invasive alien species can have complex effects on native ecosystems, and interact with multiple components of food webs, making it difficult a comprehensive quantification of their direct and indirect effects. We evaluated the relationships between the invasive crayfish, Procambarus clarkii, amphibian larvae and predatory insects, to quantify crayfish impacts on multiple levels of food webs, and to evaluate whether crayfish predation of aquatic insects has indirect consequences for their preys. We used pipe sampling to assess the abundance of crayfish, amphibian larvae and their major predators (Ditiscidae, Notonectidae and larvae of Anisoptera) in invaded and uninvaded ponds within a human dominated landscape. We disentangled the multivariate effects of P. clarkii on different components of food web through a series of constrained redundancy analyses. The crayfish had a negative, direct impact on both amphibian communities and their predators. Amphibian abundance was negatively related to both predators. However, the negative, direct effects of crayfish on amphibians were much stronger than predation by native insects. Our results suggest that this crayfish impacts multiple levels of food webs, disrupting natural prey-predator relationships.     

Factors influencing the relative abundance of invasive predators and omnivores on islands

Invasive alien species (IAS) are the major cause of native species extinctions on islands worldwide. To mitigate or eliminate IAS impacts, eradication is often the best alternative. However, IAS removal may result in cascading effects, through increase in prey abundance, mesopredator release, or competitor release. Our objective is to determine which ecological processes may influence the relative abundance of invasive carnivores and rodents on an insular system. We find that feral cat and mustelids relative abundance was strongly related by prey abundance, and for the feral cat, abundance was also controlled by habitat; these results suggest that bottom-up control through environmental filtering could be the mechanism explaining predator abundance. For rodents, we find that the abundance of the black rat was mostly controlled by the abundance of Norway rat and house mice, and food availability; the Norway rat by the abundance of black rat, a house mice and of mustelid predators; and house mouse by the other rodents and food availability. These results suggest that several mechanisms could be concurrently controlling abundance of these species; competition and predation for Norway rat, and competition and bottom-up control by environmental filtering for the other two rodents. While different factors explain the abundance of invasive species within the same functional group, food resource availability is, in general, the main controller of abundance of invasive rodents and carnivores in the Azores. Therefore, IAS management actions in these islands should focus on limiting the access to food resources and shelter, mainly near to human populations.

     

Pre-adaptive shift of a native predator (Araneae, Zodariidae) to an abundant invasive ant species (Hymenoptera, Formicidae)

Invasive species often displace native species and can affect ecological processes in invaded habitats. If invasive species become abundant, changes in prey availability may be particularly harmful to specialist predators. The Argentine ant, Linepithema humile Mayr, is an important invasive species on nearly all continents. Spiders of the genus Zodarion are specialised ant-eating predators native to the Mediterranean yet it is unknown if they can exploit invasive ant species. Here we studied spatial and temporal abundance of this invasive ant and the native spider, Zodarion cesari Pekár, during 4?years in four citrus groves. Circadian activity of both spiders and ants, and capture efficiency and prey specificity of the predator were also evaluated. The abundance of Z. cesari was strongly correlated to L. humile abundance. The predatory activity of spiders varied seasonally with differences on the relative frequency of spiders capturing ants depending on the time of the year. In laboratory, Z. cesari displayed most efficient capture upon the native ant Tapinoma nigerrimum (Nylander) and the invasive ant L. humile in comparison with five other native ant species. These results demonstrate that the native spider Z. cesari is successfully exploiting the invasive ant species L. humile and is likely a locally monophagous predator. We suggest that Z. cesari shifted away from native T. nigerrimum post invasion as both ant species are phylogenetically related and of similar size.     

Effects of invasive Pacific red lionfish Pterois volitans versus a native predator on Bahamian coral-reef fish communities

The recent irruption of Pacific red lionfish (Pterois volitans) on Caribbean and Atlantic coral reefs could prove to be one of the most damaging marine invasions to date. Invasive lionfish are reaching densities much higher than those reported from their native range, and they have a strong negative effect on the recruitment and abundance of a broad diversity of native coral-reef fishes. Otherwise, little is known about how lionfish affect native coral-reef communities, especially compared to ecologically similar native predators. A controlled field experiment conducted on small patch-reefs in the Bahamas over an 8-week-period demonstrated that (1) lionfish caused a reduction in the abundance of small native coral-reef fishes that was 2.5?±?0.5 times (mean?±?SEM) greater than that caused by a similarly sized native piscivore, the coney grouper Cephalopholis fulva (93.7 vs. 36.3?% reduction); (2) lionfish caused a reduction in the species richness of small coral-reef fishes (loss of 4.6?±?1.6 species), whereas the native piscivore did not have a significant effect on prey richness; (3) the greatest effects on the reef-fish community, in terms of both abundance and richness, occurred when both native and invasive predators were present; and (4) lionfish grew significantly faster (>6 times) than the native predator under the same field conditions. These results suggest that invasive lionfish have stronger ecological effects than similarly sized native piscivores, and may pose a substantial threat to native coral-reef fish communities.     

Threats and benefits of invasive alien plant species on pollinators

Invasive alien plant species are usually disliked due to their high pressure on native communities. However, their ecological effects on pollinators are complex: some species provide abundant floral resources, boosting the number of pollinators, while they often disrupt plant-pollinator interactions by outcompeting native plants. Our direct knowledge is mainly based on single-species studies, while understanding the mechanism of these complex ecological interactions needs multi-species field-based approaches. It is also imperative to clarify the pros and cons of invasive plants and drivers of invasion from the perspective of pollinators. We conducted a standard protocol-driven regional study in Central and Eastern Europe, comparing 6-7 invaded and non-invaded sites of 12 herbaceous invasive plant species. We sampled floral resources, bees, and hoverflies before and during the flowering of the invasive plants. We analysed the effects of plant invasion at the invasive plant species level and in combined analyses, and tested whether the life span (perennial vs. annual) and flowering time (early-, middle-, and late-flowering) of invasive plants affect the abundance, species richness, diversity and species composition of native plants and pollinators. The combined analyses showed lower abundance and species richness of flowering plants and pollinators before, and higher abundance of both during the flowering of invasive plants in invaded sites. However, invasive plants had significant species-specific effects. Perennial invasive plants had a stronger negative impact on floral resources and pollinators already before their flowering compared to annuals. Flowering time of invasive plants affected the pollinator guilds differently. We suggest that in certain critical time periods of the year, invasive plants might provide the dominant foraging resources for pollinators in an invaded ecosystem. But, they also often cause significant losses in native floral resources over the year. Instead of simple eradication, careful preparation and consideration might be needed during removal of invasive plants.     

Population and behavioural responses of native prey to alien predation

The introduction of invasive alien predators often has catastrophic effects on populations of naïve native prey, but in situations where prey survive the initial impact a predator may act as a strong selective agent for prey that can discriminate and avoid it. Using two common species of Australian small mammals that have persisted in the presence of an alien predator, the European red fox Vulpes vulpes, for over a century, we hypothesised that populations of both would perform better where the activity of the predator was low than where it was high and that prey individuals would avoid signs of the predator’s presence. We found no difference in prey abundance in sites with high and low fox activity, but survival of one species—the bush rat Rattus fuscipes—was almost twofold higher where fox activity was low. Juvenile, but not adult rats, avoided fox odour on traps, as did individuals of the second prey species, the brown antechinus, Antechinus stuartii. Both species also showed reduced activity at foraging trays bearing fox odour in giving-up density (GUD) experiments, although GUDs and avoidance of fox odour declined over time. Young rats avoided fox odour more strongly where fox activity was high than where it was low, but neither adult R. fuscipes nor A. stuartii responded differently to different levels of fox activity. Conservation managers often attempt to eliminate alien predators or to protect predator-naïve prey in protected reserves. Our results suggest that, if predator pressure can be reduced, otherwise susceptible prey may survive the initial impact of an alien predator, and experience selection to discriminate cues to its presence and avoid it over the longer term. Although predator reduction is often feasible, identifying the level of reduction that will conserve prey and allow selection for avoidance remains an important challenge.     

Food niche variation of European and American mink during the American mink invasion in north-eastern Belarus

Understanding processes allowing the co-existence of ecologically similar species is important but difficult to study in community ecology. Introductions of alien species are unplanned experiments allowing investigation of co-adaptation of both native and invasive species over a short period. We analysed food niche differentiation between native European mink and alien American mink after invasion of the latter species in Belarus. European mink feed mainly on crayfish, frogs and fish whereas American mink prefer small mammals, fish and frogs. The diet of both species varied between seasons and during the period of alien mink invasion. Concurrent with the progress of American mink invasion, the European mink food niche has narrowed to feeding mainly on frogs, with the proportion of aquatic prey (fish and crayfish) in their diet drastically reduced. In contrast, the American mink food niche became wider during invasion. The breadth was stable but included a varied proportion of different prey categories: namely an increased proportion of aquatic prey and a decreased proportion of water vole and waterfowl. The increase in abundance of American mink saw a decrease in the proportion of larger prey in their diet. When American mink preyed more often on frogs, food niche overlap of both predators increased. This result suggests that arrival of an alien competitor reduced food abundance (exploitative competition) and caused a change in native mink diet.     

Alien predators are more dangerous than native predators to prey populations

Alien predators are widely considered to be more harmful to prey populations than native predators. To evaluate this expectation, we conducted a meta-analysis of the responses of vertebrate prey in 45 replicated and 35 unreplicated field experiments in which the population densities of mammalian and avian predators had been manipulated. Our results showed that predator origin (native versus alien) had a highly significant effect on prey responses, with alien predators having an impact double that of native predators. Also the interaction between location (mainland versus island) and predator origin was significant, revealing the strongest effects with alien predators in mainland areas. Although both these results were mainly influenced by the huge impact of alien predators on the Australian mainland compared with their impact elsewhere, the results demonstrate that introduced predators can impose more intense suppression on remnant populations of native species and hold them further from their predator-free densities than do native predators preying upon coexisting prey.     

Ecological effects of invasive alien insects

A literature survey identified 403 primary research publications that investigated the ecological effects of invasive alien insects and/or the mechanisms underlying these effects. The majority of these studies were published in the last 8 years and nearly two-thirds were carried out in North America. These publications concerned 72 invasive insect species, of which two ant species, Solenopsis invicta and Linepithema humile, accounted for 18% and 14% of the studies, respectively. Most publications investigated effects on native biodiversity at population or community level. Genetic effects and, to a lesser extent, effects on ecosystem services and processes were rarely explored. We review the effects caused by different insect invaders according to: their ecosystem roles, i.e. herbivores, predators, parasites, parasitoids and pollinators; the level of biological organisation at which they occur; and the direct and indirect mechanisms underlying these effects. The best documented effects occur in invasive ants, Eurasian forest herbivores invasive in North America, and honeybees. Impacts may occur through simple trophic interactions such as herbivory, predation or parasitism. Alien species may also affect native species and communities through more complex mechanisms such as competition for resources, disease transmission, apparent competition, or pollination disruption, among others. Finally, some invasive insects, particularly forest herbivores and ants, are known to affect ecosystem processes through cascading effects. We identify biases and gaps in our knowledge of ecological effects of invasive insects and suggest further opportunities for research. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

A review on the effects of alien rodents in the Balearic (Western Mediterranean Sea) and Canary Islands (Eastern Atlantic Ocean)

Invasions of alien rodents have shown to have devastating effects on insular ecosystems. Here we review the ecological impacts of these species on the biodiversity of the Balearic and the Canary Islands. A total of seven species of introduced rodents (two rats, three mice, one dormouse, and one squirrel) have been recorded (six in the Balearics and four in the Canaries). Some of them can occasionally be important predators of nesting seabirds, contributing to the decline of endangered populations in both archipelagos. Rats are also known to prey upon terrestrial birds, such as the two endemic Canarian pigeons. Furthermore, rats actively consume both vegetative and reproductive tissues of a high number of plants, with potential relevant indirect effects on vegetation by increasing erosion and favoring the establishment of alien plants. In the Balearics, rats and mice are important seed predators of endemic species and of some plants with a restricted distribution. In the Canaries, rats intensively prey upon about half of the fleshy-fruited tree species of the laurel forest, including some endemics. In both archipelagos, alien rodents disrupt native plant–seed dispersal mutualisms, potentially reducing the chances of plant recruitment at the same time that they modify the structure of plant communities. We further suggest that alien rodents played (and play) a key role in the past and present transformation of Balearic and Canarian native ecosystems.     

Effects of invasive seaweeds on feeding preference and performance of a keystone Mediterranean herbivore

The consequences of invasive species on ecosystem processes and ecological interactions remain poorly understood. Predator–prey interactions are fundamental in shaping species evolution and community structure and can be strongly modified by species introductions. To fully understand the ecological effects of invasive species on trophic linkages it is important to characterize novel interactions between native predators and exotic prey and to identify the impacts of invasive species on the performance of native predators. Although seaweed invasions are a growing global concern, our understanding of invasive algae—herbivore interactions is still very limited. We used a series of feeding experiments between a native herbivore and four invasive algae in the Mediterranean Sea to examine the potential of native sea urchins to consume invasive seaweeds and the impacts of invasive seaweed on herbivore performance. We found that three of the four invasive species examined are avoided by native herbivores, and that feeding behaviour in sea urchins is not driven by plant nutritional quality. On the other hand, Caulerpa racemosa is readily consumed by sea urchins, but may escape enemy control by reducing their performance. Recognizing the negative impacts of C. racemosa on herbivore performance has highlighted an enemy escape mechanism that contributes to explaining how this widespread invasive alga, which is preferred and consumed by herbivores, is not eradicated by grazing in the field. Furthermore, given the ecological and economic importance of sea urchins, negative impacts of invasive seaweeds on their performance could have dramatic effects on ecosystem function and services, and should be accounted for in sea urchin population management strategies.     

Indirect ecological impacts of an invasive toad on predator–prey interactions among native species

One of the many ways that invasive species can affect native ecosystems is by modifying the behavioural and ecological interactions among native species. For example, the arrival of the highly toxic cane toad (Bufo marinus) in tropical Australia has induced toad-aversion in some native predators. Has that shift also affected the predators’ responses to native prey—for example, by reducing vulnerability of native tadpoles via a mimicry effect, or increasing vulnerability of other prey types (such as insects) via a shift in predator feeding tactics? We exposed a native predator (northern trout gudgeon, Mogurnda mogurnda) to toad tadpoles in the laboratory, and measured effects of that exposure on the fish’s subsequent intake of native tadpoles and crickets. As predicted, toad-exposed fishes reduced their rate of predation on (palatable) tadpoles of native frogs (Litoria caerulea and L. nasuta). If alternative prey (crickets) were available also, the toad-exposed fishes shifted even more strongly away from predation on native tadpoles. Thus, invasion of a toxic species can provide a mimicry benefit to native taxa that resemble the invader, and can shift predation pressure onto other taxa.     

Experimental Test of Preferences for an Invasive Prey by an Endangered Predator: Implications for Conservation

Identifying impacts of exotic species on native populations is central to ecology and conservation. Although the effects of exotic predators on native prey have received much attention, the role of exotic prey on native predators is poorly understood. Determining if native predators actively prefer invasive prey over native prey has implications for interpreting invasion impacts, identifying the presence of evolutionary traps, and predator persistence. One of the world’s most invasive species, Pomacea maculata, has recently established in portions of the endangered Everglade snail kite’s (Rostrhamus sociabilis plumbeus) geographic range. Although these exotic snails could provide additional prey resources, they are typically much larger than the native snail, which can lead to lower foraging success and the potential for diminished energetic benefits in comparison to native snails. Nonetheless, snail kites frequently forage on exotic snails. We used choice experiments to evaluate snail kite foraging preference in relation to exotic species and snail size. We found that snail kites do not show a preference for native or exotic snails. Rather, snail kites generally showed a preference for medium-sized snails, the sizes reflective of large native snails. These results suggest that while snail kites frequently forage on exotic snails in the wild, this behavior is likely driven simply by the abundance of exotic snails rather than snail kites preferring exotics. This lack of preference offers insights to hypotheses regarding effects of exotic species, guidance regarding habitat and invasive species management, and illustrates how native-exotic relationships can be misleading in the absence of experimental tests of such interactions.     

Naïveté in novel ecological interactions: lessons from theory and experimental evidence

The invasion of alien species into areas beyond their native ranges is having profound effects on ecosystems around the world. In particular, novel alien predators are causing rapid extinctions or declines in many native prey species, and these impacts are generally attributed to ecological naïveté or the failure to recognise a novel enemy and respond appropriately due to a lack of experience. Despite a large body of research concerning the recognition of alien predation risk by native prey, the literature lacks an extensive review of naïveté theory that specifically asks how naïveté between novel pairings of alien predators and native prey disrupts our classical understanding of predator–prey ecological theory. Here we critically review both classic and current theory relating to predator–prey interactions between both predators and prey with shared evolutionary histories, and those that are ecologically ‘mismatched’ through the outcomes of biological invasions. The review is structured around the multiple levels of naïveté framework of Banks & Dickman (2007), and concepts and examples are discussed as they relate to each stage in the process from failure to recognise a novel predator (Level 1 naïveté), through to appropriate (Level 2) and effective (Level 3) antipredator responses. We discuss the relative contributions of recognition, cue types and the implied risk of cues used by novel alien and familiar native predators, to the probability that prey will recognise a novel predator. We then cover the antipredator response types available to prey and the factors that predict whether these responses will be appropriate or effective against novel alien and familiar native predators. In general, the level of naïveté of native prey can be predicted by the degree of novelty (in terms of appearance, behaviour or habitat use) of the alien predator compared to native predators with which prey are experienced. Appearance in this sense includes cue types, spatial distribution and implied risk of cues, whilst behaviour and habitat use include hunting modes and the habitat domain of the predator. Finally, we discuss whether the antipredator response can occur without recognition per se, for example in the case of morphological defences, and then consider a potential extension of the multiple levels of naïveté framework. The review concludes with recommendations for the design and execution of naïveté experiments incorporating the key concepts and issues covered here. This review aims to critique and combine classic ideas about predator–prey interactions with current naïveté theory, to further develop the multiple levels of naïveté framework, and to suggest the most fruitful avenues for future research.     

Assessing the risk effects of native predators on the exotic American bullfrog (Lithobates catesbeianus) and their indirect consequences to ecosystem function

Understanding the factors and mechanisms that affect the impacts of invasive species in invaded environments has been widely debated among researchers. However, few studies about invasive species have explored the effects of predation risks by native predators on exotic prey. Herein, the traditional invasive predator-native prey framework was reversed. We tested if tadpoles, of the worldwide invasive American Bullfrog Lithobates catesbeianus, were affected by the predation risk imposed by native predators. We used two different species of belostomatid predators and tested whether and how predation-induced phenotypic plasticity on L. catesbeianus reverberated in morphological, physiological, and ecosystem-level processes. Individuals of L. catesbeianus modified their morphological (tail muscle width), behavioral (activity and foraging), and physiological (growth and growth efficiency) traits in the presence of predation risk. Based on the observed morphological changes, our results suggest that prey may recognize predator-specific cues. In addition, we observed that L. catesbeianus' responses to predation risk can affect ecosystem-level properties, by inducing trophic cascades and reducing animal-mediated nutrient recycling rates. In summary, our study supports that exotic prey species who are subjected to native predators may display anti-predator responses, with implications for their development, as well as possible ecosystem-level effects.     

Native predator eats invasive toxic prey: evidence for increased incidence of consumption rather than aversion-learning

Contemporary adaptation of native prey species to invasive predators has been relatively well documented, but that of native predators to invasive prey has received less attention. Because the level of impact an invasive species will have on its predators versus its prey will determine changes in community trophic structure, it is important to understand how native predators respond to novel prey. Here we examine the response of native fence lizards to the invasion of red imported fire ants, a novel toxic prey. Examining invaded and uninvaded lizard populations, we tested whether or not aversion-learning occurs in juvenile fence lizards over successive feedings (within lifetime), how previous fire ant exposure may affect avoidance behavior (over generations), and whether population differences are consistent when prey choice exists. We also examine rates of phenotypic divergence in traits associated with the native species as both predator and prey. Aversion-learning did not occur in either population. Instead, the incidence of fire ant consumption increased over both successive feedings and generations. Lizards from the fire ant invaded population had a higher propensity to eat fire ants than fire ant-naïve lizards, even when given a choice between prey items. We found greater phenotypic divergence in traits associated with the native species as predator on, versus as prey to, fire ants. Although the strategy of eating these novel toxic prey can impose survival costs in the short term, over the longer-term, eating fire ants may cost little or even benefit survivors.     

Relative abundance of an invasive alien plant affects native pollination processes

One major characteristic of invasive alien species is their occurrence at high abundances in their new habitat. Flowering invasive plant species that are visited by native insects and overlap with native plant species in their pollinators may facilitate or disrupt native flower visitation and fertilisation by forming large, dense populations with high numbers of flowers and copious rewards. We investigated the direction of such a proposed effect for the alien invasive Rhododendron ponticum in Irish habitats. Flower visitation, conspecific and alien pollen deposition, fruit and seed set were measured in a self-compatible native focal plant, Digitalis purpurea, and compared between field sites that contained different relative abundances of R. ponticum. Flower visitation was significantly lower at higher alien relative plant abundances than at lower abundances or in the absence of the alien. Native flowers experienced a significant decrease in conspecific pollen deposition with increasing alien abundance. Heterospecific pollen transfer was very low in all field sites but increased significantly with increasing relative R. ponticum abundance. However, lower flower visitation and lower conspecific pollen transfer did not alter reproductive success of D. purpurea. Our study shows that indirect interactions between alien and native plants for pollination can be modified by population characteristics (such as relative abundance) in a similar way as interactions among native plant species. In D. purpurea, only certain aspects of pollination and reproduction were affected by high alien abundances which is probably a result of high resilience due to a self-compatible breeding system. Native species that are more susceptible to pollen limitation are more likely to experience fitness disadvantages in habitats with high relative alien plant abundances.