A review of mammal eradications on Mediterranean islands

1. Impacts of alien invasive species on island communities and ecosystems may be even more detrimental than on the mainland. Therefore, since the 1950s, hundreds of restoration projects have been implemented worldwide, with the aim of controlling or eradicating alien species from islands. To date, no review has been focused on eradication on Mediterranean islands. To fill the gap, I reviewed the available information concerning mammal eradications so far carried out on Mediterranean islands, examining the details of several aspects of project implementation and monitoring.
2. I obtained data for 139 attempted eradications on 107 Mediterranean islands in eight countries, with Greece, Italy, and Spain accounting for the highest number. Eradication projects targeted 13 mammal species. The black rat Rattus rattus was the target of over 75% of the known attempted eradications in the Mediterranean Basin; other species targeted were feral goat Capra hircus, house mouse Mus musculus, European rabbit Oryctolagus cuniculus, and domestic cat Felis catus. The most widely adopted technique was poisoning (77% of all eradications), followed by trapping (15%) and hunting (4%). However, techniques were largely target-specific.
3. The average failure rate was about 11%. However, this percentage varied according to the specific mammalian order, and eradications of Carnivora failed more often than those of other mammals. Among rodents, house mouse eradication attained a very high failure rate (75%). Reinvasion occurred after 15% of successful eradications.
4. A better understanding of the motivations of animal rights activists may improve the chance of success when eradicating charismatic or domesticated species. Furthermore, it is crucial to collect data and case studies about reinvasions, in order to strengthen biosecurity programmes following eradication. As in other parts of the world, the next frontier in alien mammal management on Mediterranean islands concerns the eradication of invasive species from inhabited islands.

     

Trophic niche changes associated with the eradication of invasive mammals in an insular lizard: an assessment using isotopes

Invasive species are a major threat to island biodiversity, and their eradications have substantially contributed to the conservation of island endemics. However, the consequences of eradications on the trophic ecology of native taxa are largely unexplored. Here, we used the eradication of invasive black rats Rattus rattus and European rabbits Oryctolagus cuniculus from the Berlenga Island, in the western coast of Portugal, as a whole-ecosystem experiment to investigate the effects of the eradication of invasive mammals on the trophic niche and body dimensions of the island-restricted Berlenga wall lizard Podarcis carbonelli berlengensis over a 2-year period. Our results suggest an expansion of the isotopic niche and an intensification of the sexual dimorphism of the lizard following mammal eradication. Additionally, we found considerable variability in isotopic niche across the island and detected evidence of sex-specific and season-modulated nutritional requirements of this threatened reptile. Our findings support that the eradication of 2 of the planet’s most problematic invasive vertebrates led to changes in the lizard trophic niche and sexual dimorphism in just 2 years. This suggests that the ecological pressures—for example, prey availability and habitat structure—to which lizards are exposed have substantially changed post-eradication. Our study emphasizes the scientific value of island eradications as experiments to address a wide range of ecological questions and adds to the increasing body of evidence supporting substantial conservation gains associated with these restoration interventions.     

Propagule pressure determines recruitment from a commercial shipping pier

Artificial structures associated with shipping and boating activities provide habitats for a diverse suite of non-indigenous marine species. Little is known about the proportion of invader success in nearby waters that is attributable to these structures. Areas close to piles, wharves and piers are likely to be exposed to increasing levels of propagule pressure, enhancing the recruitment of non-indigenous species. Recruitment of non-indigenous and native marine biofouling taxa were evaluated at different distances from a large commercial shipping pier. Since artificial structures also represent a desirable habitat for fish, how predation on marine invertebrates influences the establishment of non-indigenous and native species was also evaluated. The colonisation of several non-indigenous marine species declined rapidly with distance from the structure. Little evidence was found to suggest that predators have much influence on the colonisation success of marine sessile invertebrate species, non-indigenous or otherwise. It is suggested that propagule pressure, not predation, more strongly predicts establishment success in these biofouling assemblages.     

Holocene turnover of the French vertebrate fauna

Comparing available paleontological, archaeological, historical, and former distributional data with current natural history and distributions demonstrated a turnover in the French vertebrate fauna during the Holocene (subdivided into seven sub-periods). To this end, a network of 53 specialists gleaned information from more than 1300 documents, the majority never cited before in the academic literature. The designation of 699 species as native, vanished, or non-indigenous in France or in one or more of its biogeographical entities during the Holocene period was investigated. Among these 699 species, 585 were found to belong to one or more of these categories. Among the 154 species that fit the definition of non-indigenous, 86 species were new species for France during the Holocene. Fifty-one that were autochthonous vanished from France during this period. Among these 51 species, 10 (two birds and eight mammals) are now globally extinct. During the last 11 millennia, the turnover in the French vertebrate fauna yielded a net gain of 35 species. On a taxon-by-taxon basis, there was a gain in the sizes of the ichthyofauna (19 : 27%), the avifauna (10 : 3%) and the herpetofauna (7 : 9%) and a loss in the mammalian fauna (−1 : 1%). Values of a per-century invasion index were less than 1 between 9200 BC and 1600 AD but increased dramatically after this date. An exponential model fits the trajectory of this index well, reaching the value of 132 invasions per century for the last sub-period, which encompasses 1945–2002. Currently, the local ecological and economic impacts of populations of 116 species (75% of the 154 that satisfied the criteria for non-indigenous) are undocumented, and the non-indigenous populations of 107 vertebrate species (69%) are unmanaged. The delay in assessing the ecological and economical impact of non-indigenous species, which is related to a lack of interest of French academic scientists in the Science and Action programmes, prevents the public from becoming informed and hinders the debates needed to construct a global strategy. For such a strategy to be effective, it will have to be elaborated at a more global scale than in just France – definitely at least in Europe. This revised version was published online in July 2006 with corrections to the Cover Date.     

Costing eradications of alien mammals from islands

The ability to estimate costs of alien species eradications is essential for a rigorous assessment of priorities for island restoration. Using a global data file from 41 islands, mostly gleaned from the 'grey' literature, we show that the cost of vertebrate eradications can be satisfactorily predicted if island area and species to be eradicated are known. About 72% of the variation in cost can be explained by island area, whereas, for a given area, rodent eradications are 1.7–3.0 times more expensive than ungulate eradications. Costs per hectare decrease with island size. Restricting the analysis to roughly half the data set, the relatively homogeneous half concerned with New Zealand islands, we identify two further influences on cost: date of eradication and distance to the main airport (an indicator of remoteness). For a given area, costs have declined over time but increase with island remoteness. This information therefore provides conservation planners with a robust, if preliminary, estimate of the cost of any proposed eradication programme.     

Patterns of Biological Invasions in French Freshwater Systems by Non-Indigenous Macroinvertebrates

Freshwater biodiversity is threatened by several mechanisms, of which the introduction of non-indigenous species and habitat alteration are the two most important. Exotic species act at various levels of organisation of macroinvertebrate communities, and are involved in different processes mediating their impacts on biodiversity, such as habitat modification or negative interactions with autochthonous fauna. The present work gives a list of the 43 French freshwater non-indigenous species, which represent 1.2% of the French freshwater macroinvertebrates. We provide their geographic origins, their distributions among zoological units by comparison with the native fauna and their functional characteristics according to a recent typology based on bio/ecological traits. An exponential trend of the cumulated number of non-indigenous species was evidenced, with a clumping of invaders within crustaceans and molluscs. Donor areas of non-indigenous species are in majority European, and the Ponto-Caspian basin is identified as the principal one. This pattern could be explained by a spread along waterways but its origin lies in a process of recolonisation of defaunated areas following several episodes of glaciation/deglaciation in Western Europe during the last 80,000 years. Finally, from a functional point of view, non-indigenous species exhibit a limited diversity, with two functional groups representing 80% of them.     

Estimating realistic costs for strategic management planning of invasive species eradications on islands

Environmental managers regularly face decisions about how to counteract threats. These decisions require an understanding of both the conservation benefits and economic costs of candidate actions. However, transparent frameworks for how to accurately calculate costs for management are rare. We worked with island managers in Australia to develop eradication protocols for six invasive species- four mammals and two weeds. We used the protocols to create an accounting framework for invasive species eradications to produce realistic cost estimates for eradications across multiple locations. We also used our models to test common cost assumptions: (1) that costs scale linearly with area, (2) that terrain does not influence costs, and (3) that eradication costs stay constant through time. By explicating testing assumptions, we found that costs largely scaled linearly with area, that terrain influences costs, and that costs decline as populations decline in response to ongoing management. Estimated mammal eradication costs were driven in large part by the area of an island and the cost of transport. However, when area alone was used as a proxy for costs, the calculated costs deviated from our modelled costs by 40–56%. Weed eradication cost estimates were driven by the size and density of an infestation as well as the terrain of the island, with the effect of terrain becoming more pronounced as area to be treated increased. We provide a method to calculate realistic costs across several sites, which can be used to guide strategic management decision-making, including prioritisation, and on-ground management actions.     

Eradications of invasive alien species in Europe: a review

Eradication of alien species is a key conservation tool to mitigate the impacts caused by biologic invasions. The aim of the present paper is to review the eradications successfully completed in Europe and to discuss the main limits to a wider application of this management option in the region. On the basis of the available literature – including conference proceedings, national reports to the Bern Convention, etc. – a total of 37 eradication programmes have been recorded. Thirty-three eradications were carried out on islands and four on the mainland. The rat (Rattus spp.) has been the most common target (n = 25, 67%), followed by the rabbit (n = 4). In many cases, these eradications determined a significant recovery of native biodiversity. Differently to other regions of the world, no eradications of alien invertebrates and marine organisms have been recorded; regarding invasive alien plants, it appears that only some very localized removals have been completed so far in Europe. The limited number of eradications carried out in Europe so far is probably due to the limited awareness of the public and the decision makers, the inadequacy of the legal framework, and the scarcity of resources. Synthetic guidelines for improving the ability of European states to respond to aliens incursions are presented. This revised version was published online in July 2006 with corrections to the Cover Date.     

Prioritising islands in the United Kingdom and crown dependencies for the eradication of invasive alien vertebrates and rodent biosecurity

Invasive alien vertebrates (IAVs) pose a significant threat to island biodiversity worldwide, and their removal is an important nature conservation management goal. As methods advance, eradications from larger islands and of multiple species simultaneously are increasingly undertaken. Effective targeting to maximise conservation gain is important given limited resources. We build on existing prioritisation methods and use the islands of the UK and Crown Dependencies (UK) as an example of how vertebrate eradications might be prioritised and invasive-free status maintained through biosecurity. For each of the 9688 UK islands, we assessed ecological importance for native vertebrates and the anticipated impacts of the IAVs present to estimate the benefit of restoration based on the feasibility and sustainability of IAV eradications in relation to island size, human population and risk of unassisted reinvasion by swimming. As reinvasion poses a threat to the long-term benefits of eradication, we incorporated species-specific swimming distances and explored the effects of varying reinvasion probability from risk-averse to higher-risk strategies. The 25 islands that would benefit most from eradications were in Scotland, Northern Ireland and the Channel Islands. Our prioritisation method should be seen as an initial guide to identify islands that might benefit from intervention when faced with a large list of potential sites. Feasibility studies taking account of factors such as interspecific interactions, anthropogenic reinvasion, views of residents or ‘social feasibility’ and cost need to be undertaken before planning any eradication. We prioritised biosecurity for rat-free islands to highlight where comprehensive measures might be most beneficial.     

Avoiding surprise effects on Surprise Island: alien species control in a multitrophic level perspective

Eradications of invasive alien species have generally benefited biodiversity. However, without sufficient planning, successful eradications can have unexpected and unwanted consequences for native species and ecosystems. In particular, the “surprise effect” is the rapid increase of hitherto unnoticed species following the sudden removal of an invasive alien that was exerting an ecological force on those species (predation, competition or herbivory, for example). The only way to prevent these undesired outcomes is to adapt the control programme following the characterization of the trophic relationships between the invasive alien species and the invaded communities, that is, to view the control with a holistic perspective. Here, we illustrate this point with the study of the role of the ship rat (Rattus rattus), which invaded a tropical pacific atoll, Surprise Island, New Caledonia. We assessed the risk of surprise effects during a pre-eradication phase of several years, and then adapted our eradication strategy accordingly.     

Eradication of populations of an invasive ant in northern Australia: successes, failures and lessons for management

Eradication is the most difficult management goal for exotic species, and successes are rare and even more rarely published. The lack of publication of the methodology and outcomes of eradication programs severely limits the transfer of knowledge to programs elsewhere that target the same or similar species. Here I detail the successes and failures of eradication efforts on six populations of African big headed ant Pheidole megacephala in northern Australia, covering a combined area of almost 9 ha. Two years post-treatment, assessment criteria for successful eradication were met for four of the six populations, whereas eradication failed in the remaining two, resulting in the need for ongoing management. Positive outcomes are attributed to eight criteria being met: (1) a single line of project management authority; (2) over-arching legal authority; (3) susceptibility of the target organism to control procedures; (4) sufficient resources; (5) detectibility of the target organism at low densities; (6) early intervention; (7) prevention of reinvasion; and (8) prevention of invasive succession. Reasons for one of the failures remain unclear, but eradication failed in the other because a part of the population was not treated. In both cases, the eradication failures could have been detected and managed much earlier than was the case. The successes and lessons documented here, coupled with the now large number of small-scale eradications of this ant, warrant the implementation of larger and more ambitious management programs against this significant invader, especially within areas of high conservation value.     

Invasive legume management strategies differentially impact mutualist abundance and benefit to native and invasive hosts

Determining the best management practices for plant invasions is a critical, but often elusive goal. Invasive removals frequently involve complex and poorly understood biotic interactions. For example, invasive species can leave potent legacies that influence the success of native species restoration efforts, and positive plant‐microbial feedbacks may promote continued reinvasion by an exotic species following restoration. Removal methods can vary in their effects on plant–soil feedbacks, with consequences for restoration of native species. We determined the effects of invasion by a leguminous shrub (French broom; Genista monspessulana) on the density and community composition of, and benefit conferred by, its microbial mutualists in its invading range. Densities of soil‐dwelling rhizobia were much higher in areas invaded by G. monspessulana relative to uninvaded areas, and this increased density of rhizobia fed back to increase seedling growth of both the invader and native legumes. We further compared how three techniques for removing G. monspessulana affected the densities of rhizobia relative to areas where G. monspessulana was still present. Removal by hand‐pulling reduced soil rhizobial densities, and reduced growth of one native legume, while having no effect on the growth of the invader. Overall, our results show that the consequences of restoration techniques, both above‐ and belowground, could be critical for the successful removal of an invasive legume and restoration of native species.     

The Importance of Detritivore Species Diversity for Maintaining Stream Ecosystem Functioning Following the Invasion of a Riparian Plant

The strength of linkages between riparian plants and stream communities can be expected to be influenced by invading plants. While most studies so far have been focussed on the effects of the leaf litter quality of the invader, this study addresses the impact of detritivores on the pool of detritus. In a natural setting, we found that species richness of shredding macroinvertebrates significantly influenced the breakdown rate of an invasive weed species, the Japanese knotweed (Fallopia japonica), which has become a major plant invader along streams and rivers in Europe and North America. Our findings imply that a reduction of the diversity of shredder species, which may be the result of disturbances, could negatively influence stream ecosystems' capacity of processing knotweed leaves. Although the knotweed showed breakdown rates similar to those of common native tree and shrub species, other exotic leaf species might show considerably slower rates and hence have greater consequences for the ecosystems. We have, in this study, indicated a technique by which the effects of other non-indigenous plants on ecosystem functioning might be considered.     

Many eyes on the ground: citizen science is an effective early detection tool for biosecurity

Early detection of target non-indigenous species is one of the most important determinants of a successful eradication campaign. For early detection to be successful, and provide the highest probability of achieving eradication, intense surveillance is often required that can involve significant resources. Volunteer based monitoring or “citizen science” is one potential tool to address this problem. This study differs from standard citizen science projects because the participants are personnel or contractors of a company working on Barrow Island, Western Australia. We show that personnel can contribute successfully to a surveillance program aimed at detecting a broad taxonomic range of non-indigenous vertebrate and invertebrate species. Using data collected over a five year surveillance period on Barrow Island, we show that eighteen of the nineteen (95%) non-indigenous invertebrate species new to the island were detected by personnel working on the island, and that the number of detections made by these workers was significantly related to the number of personnel on the island at any one time. Most personnel detections (91%) were made inside buildings where the majority of active surveillance tools could not be implemented. For vertebrates, 4 NIS species detections (100% of detections) were made in the built environment by personnel. Although reporting of suspect non-indigenous species is voluntary, personnel are required to attend inductions and toolboxes where reporting of suspect biosecurity risk material is encouraged. These results demonstrate the value of industry led ‘citizen science’ programs, resulting in sustained stewardship and conservation of areas with high environmental value.     

Eradicating multiple invasive species on inhabited islands: the next big step in island restoration?

Invasive species are the greatest threat to island ecosystems, which harbour nearly half the world’s endangered biodiversity. However, eradication is more feasible on islands than on continents. We present a global analysis of 1,224 successful eradications of invasive plants and animals on 808 islands. Most involve single vertebrate species on uninhabited islands, but plant and invertebrate eradications occur more often on inhabited islands. Inhabited islands are often highly modified and support numerous introduced species. Consequently, targeting a single invasive species can be ineffective or counterproductive. The impacts of other pests will continue and, in some cases, be exacerbated. The presence of people also creates regulatory, logistical and socio-political constraints. Real or perceived health risks to inhabitants, pets and livestock may restrict the use of some eradication tools, and communities or individuals sometimes oppose eradication. Despite such challenges, managing invasive species is vital to conserve and restore the unique biodiversity of many inhabited islands, and to maintain or improve the welfare and livelihoods of island residents. We present a brief case study of the Juan Fernández Archipelago, Chile, and discuss the feasibility of eradicating large suites of invasive plants and animals from inhabited islands while managing other invaders for which eradication is not feasible or desirable. Eradications must be planned to account for species interactions. Monitoring and contingency plans must detect and address any ‘surprise effects’. Above all, it is important that the local community derives social, cultural and/or economic benefits, and that people support and are engaged in the restoration effort.     

Carrion fly‐derived DNA metabarcoding is an effective tool for mammal surveys: Evidence from a known tropical mammal community

Metabarcoding of vertebrate DNA derived from carrion flies has been proposed as a promising tool for biodiversity monitoring. To evaluate its efficacy, we conducted metabarcoding surveys of carrion flies on Barro Colorado Island (BCI), Panama, which has a well‐known mammal community, and compared our results against diurnal transect counts and camera trapping. We collected 1,084 flies in 29 sampling days, conducted metabarcoding with mammal‐specific (16S) and vertebrate‐specific (12S) primers, and sequenced amplicons on Illumina MiSeq. For taxonomic assignment, we compared blast with the new program protax , and we found that protax improved species identifications. We detected 20 mammal, four bird, and one lizard species from carrion fly metabarcoding, all but one of which are known from BCI. Fly metabarcoding detected more mammal species than concurrent transect counts (29 sampling days, 13 species) and concurrent camera trapping (84 sampling days, 17 species), and detected 67% of the number of mammal species documented by 8 years of transect counts and camera trapping combined, although fly metabarcoding missed several abundant species. This study demonstrates that carrion fly metabarcoding is a powerful tool for mammal biodiversity surveys and has the potential to detect a broader range of species than more commonly used methods.     

Invasive Ponto-Caspian Amphipods and Fish Increase the Distribution Range of the Acanthocephalan Pomphorhynchus tereticollis in the River Rhine

Non-indigenous species that become invasive are one of the main drivers of biodiversity loss worldwide. In various freshwater systems in Europe, populations of native amphipods and fish are progressively displaced by highly adaptive non-indigenous species that can perform explosive range extensions. A total of 40 Ponto-Caspian round gobies Neogobius melanostomus from the Rhine River near Düsseldorf, North Rhine-Westphalia, Germany, were examined for metazoan parasites and feeding ecology. Three metazoan parasite species were found: two Nematoda and one Acanthocephala. The two Nematoda, Raphidascaris acus and Paracuaria adunca, had a low prevalence of 2.5%. The Acanthocephala, Pomphorhynchus tereticollis, was the predominant parasite species, reaching a level of 90.0% prevalence in the larval stage, correlated with fish size. In addition, four invasive amphipod species, Corophium curvispinum (435 specimens), Dikerogammarus villosus (5,454), Echinogammarus trichiatus (2,695) and Orchestia cavimana (1,448) were trapped at the sampling site. Only D. villosus was infected with P. tereticollis at a prevalence of 0.04%. The invasive goby N. melanostomus mainly preys on these non-indigenous amphipods, and may have replaced native amphipods in the transmission of P. tereticollis into the vertebrate paratenic host. This study gives insight into a potential parasite-host system that consists mainly of invasive species, such as the Ponto-Caspian fish and amphipods in the Rhine. We discuss prospective distribution and migration pathways of non-indigenous vertebrate (round goby) and invertebrates (amphipods) under special consideration of parasite dispersal.     

Native seed addition as an effective tool for post-invasion restoration

Invasive plant species reduce biodiversity, alter ecosystem processes, and cause economic losses. Control of invasive plants is therefore highly desired by land managers and policy makers. However, invasive plant control strategies frequently fail, partly because management often concentrates only on the eradication of invasive plants and not on revegetation with native species that use the available resources and prevent reinvasion. In this study, we focused on the intracontinental invader Rumex alpinus L., which was introduced by humans from the Alps to the lower mountains of Central Europe, where it has spread to semi-natural meadows, suppresses local biodiversity, and reduces the quality of hay used as cattle fodder. The species can be effectively removed using herbicide, but this leaves behind a persistent seed bank. Without further treatment, the invader rapidly regenerates and reinvades the area. We supplemented the herbicide treatment by adding the seeds of native grasses. Addition of native-seed effectively suppressed the regeneration of the invader from the seed bank, reduced its biomass, and consequently, prevented massive reinvasion. While the invader removal was successful, the restored community remained species-poor because the dense sward of native grasses blocked the regeneration of native forbs from the seed bank. Nevertheless, the addition of native seed proved to be an effective tool in preventing reinvasion after the eradication of the invasive plant.     

The illusion of nature: perception and the reality of natural landscapes,as illustrated by vertebrate fauna in the Northern Territory,Australia

Biomass figures are compared for common native vertebrate species and common non‐native vertebrate species (including fish, amphibian, reptile, bird and mammal species) across the Northern Territory, an area of ostensibly, largely unmodified natural system. The total biomass of the considered non‐native species very substantially surpasses that of the common native vertebrate species considered; hence, the perception that this is a largely intact natural system is, to some extent, an illusion. This preponderance of biomass of non‐native species may help explain the increasing evidence of ecosystem stress and decline of native species. An integrity index based on the relative biomass of native and non‐native species may provide insight into the status and trends of ecological systems across different regions.     

Vertebrate invaders and their ecological impacts in Chile

The South American country of Chile has been subjected to relatively few invasions in historic times. In comparison to the ca 610 vertebrate species found in continental Chile, only 24 species (3.9%) have invaded the country. Except for two bird and two or three mammal species that expanded their range and crossed the Andean Ranges from Argentina, the remaining 20 species were all introduced, or aided, by humans. Of the 24 invader species that currently occur in Chile, 11 (46%) were first introduced in central Chile, two (8%) in the northern part of the country, nine (38%) in the southern part, and two (8%) in Juan Fernández Archipelago. For ten (42%) of those species there is no information about their effects on the native flora, vegetation, or fauna. For eight species (33%), the information regarding the effects of the invaders is anecdotal. For six species (25%), there is adequate quantitative documentation available on their effects. Of a total of seven convincingly repo rted cases, two involve positive effects (increase in the prey base for native predators) and five have negative effects, of which three are on native vegetation and the remaining two on native fauna.