Michel Pascal

Impacts of biological invasions: what's what and the way forward

Study of the impacts of biological invasions, a pervasive component of global change, has generated remarkable understanding of the mechanisms and consequences of the spread of introduced populations. The growing field of invasion science, poised at a crossroads where ecology, social sciences, resource management, and public perception meet, is increasingly exposed to critical scrutiny from several perspectives. Although the rate of biological invasions, elucidation of their consequences, and knowledge about mitigation are growing rapidly, the very need for invasion science is disputed. Here, we highlight recent progress in understanding invasion impacts and management, and discuss the challenges that the discipline faces in its science and interactions with society.

Mammal invaders on islands: impact, control and control impact

The invasion of ecosystems by exotic species is currently viewed as one of the most important sources of biodiversity loss. The largest part of this loss occurs on islands, where indigenous species have often evolved in the absence of strong competition, herbivory, parasitism or predation. As a result, introduced species thrive in those optimal insular ecosystems affecting their plant food, competitors or animal prey. As islands are characterised by a high rate of endemism, the impacted populations often correspond to local subspecies or even unique species. One of the most important taxa concerning biological invasions on islands is mammals. A small number of mammal species is responsible for most of the damage to invaded insular ecosystems: rats, cats, goats, rabbits, pigs and a few others. The effect of alien invasive species may be simple or very complex, especially since a large array of invasive species, mammals and others, can be present simultaneously and interact among themselves as well as with the indigenous species. In most cases, introduced species generally have a strong impact and they often are responsible for the impoverishment of the local flora and fauna. The best response to these effects is almost always to control the alien population, either by regularly reducing their numbers, or better still, by eradicating the population as a whole from the island. Several types of methods are currently used: physical (trapping, shooting), chemical (poisoning) and biological (e.g. directed use of diseases). Each has its own set of advantages and disadvantages, depending on the mammal species targeted. The best strategy is almost always to combine several methods. Whatever the strategy used, its long‐term success is critically dependent on solid support from several different areas, including financial support, staff commitment, and public support, to name only a few. In many cases, the elimination of the alien invasive species is followed by a rapid and often spectacular recovery of the impacted local populations. However, in other cases, the removal of the alien is not sufficient for the damaged ecosystem to revert to its former state, and complementary actions, such as species re‐introduction, are required. A third situation may be widespread: the sudden removal of the alien species may generate a further disequilibrium, resulting in further or greater damage to the ecosystem. Given the numerous and complex population interactions among island species, it is difficult to predict the outcome of the removal of key species, such as a top predator. This justifies careful pre‐control study and preparation prior to initiating the eradication of an alien species, in order to avoid an ecological catastrophe. In addition, long‐term monitoring of the post‐eradication ecosystem is crucial to assess success and prevent reinvasion.

Island colonization and founder effects: the invasion of the Guadeloupe islands by ship rats (Rattus rattus)

The stepwise colonization of islands within an archipelago is typically punctuated by successive founder effects, with each newly founded population being a subsample of the gene pool of the source island. Thus, the genetic signature of successive bottlenecks should be detected when analysing the genetic structure between islands of an archipelago. To test this prediction, we investigated introduced ship rat populations, Rattus rattus (Linnaeus, 1758), in the Guadeloupe Archipelago. Three different methods, commonly named the heterozygosity excess, the mode‐shift indicator and the M ratio method, were used to detect bottlenecks from genetic data obtained with eight microsatellite markers on Guadeloupe and two neighbouring islands, Petite‐Terre and Fajou. Moreover, a recent eradication failure on Fajou allowed us to test the accuracy of the methods in an ‘experimental‐like’ situation. The results indicate that rats were introduced on Guadeloupe first, which then became the source population for independent secondary colonization of Fajou and Petite‐Terre. Moreover, the heterozygosity excess and the mode‐shift indicator only detected bottlenecks for the recent colonization of Petite‐Terre and the eradication failure on Fajou. However, bottlenecks were detected for all the populations using the M ratio method. This could be interpreted as the remaining signature of the early introduction of the ship rat in the archipelago.

French attempts to eradicate non-indigenous mammals and their consequences for native biota

Many European politicians, managers, and scientists believe that non-indigenous species cannot be eradicated and that attempts to do so are hazardous because of frequent undesirable results. This notion seems to be based on the view that successful eradications undertaken in many other parts of the world cannot be generalised. To allow reasoned consideration of this argument, the eradication of non-indigenous vertebrate species performed in the French territories (European and overseas) and their recorded consequences on native fauna and flora are synthesised. Nineteen vertebrate eradication attempts were recorded, with seven mammal species as the targets. Of these attempts four failed for technical reasons and one for reasons undetermined as yet. These operations took place on islands of four biogeographical areas (West-European, Mediterranean, West Indies and Indian Ocean subantarctic) except a continental one (West-European continent). Among these 19 attempts, 13 were conducted according to a global strategy that provided data on the impact of the disappearance of the non-indigenous species on several native species. This impact, never detrimental, was determined for 14 species (one mammal, nine birds, one marine turtle, one crab, one beetle, one plant). Unexpected consequences of the disappearance of the invader were recorded for four native species (29%). This result highlights the poverty of natural historical information for several taxa and the flimsiness of the empty niche concept that is often used to argue for the delay of or to prevent any action again a non-indigenous species. If French territories can be taken as an example, eradications of non-indigenous species are not impossible; a good risk assessment prevents undesirable long-term consequences for native species and several native species benefited from the disappearance of the invader. Furthermore, eradication constitutes a powerful experimental tool for ecology and natural history studies if conceived as both a management and research operation.

Divergent evolutionary processes associated with colonization of offshore islands

Oceanic islands have been a test ground for evolutionary theory, but here, we focus on the possibilities for evolutionary study created by offshore islands. These can be colonized through various means and by a wide range of species, including those with low dispersal capabilities. We use morphology, modern and ancient sequences of cytochrome b (cytb) and microsatellite genotypes to examine colonization history and evolutionary change associated with occupation of the Orkney archipelago by the common vole (Microtus arvalis), a species found in continental Europe but not in Britain. Among possible colonization scenarios, our results are most consistent with human introduction at least 5100 bp (confirmed by radiocarbon dating). We used approximate Bayesian computation of population history to infer the coast of Belgium as the possible source and estimated the evolutionary timescale using a Bayesian coalescent approach. We showed substantial morphological divergence of the island populations, including a size increase presumably driven by selection and reduced microsatellite variation likely reflecting founder events and genetic drift. More surprisingly, our results suggest that a recent and widespread cytb replacement event in the continental source area purged cytb variation there, whereas the ancestral diversity is largely retained in the colonized islands as a genetic ‘ark’. The replacement event in the continental M. arvalis was probably triggered by anthropogenic causes (land‐use change). Our studies illustrate that small offshore islands can act as field laboratories for studying various evolutionary processes over relatively short timescales, informing about the mainland source area as well as the island.

Invasive rats and seabirds after 2,000 years of an unwanted coexistence on Mediterranean islands

In the Mediterranean, the survival of endemic long-lived seabirds despite the long-standing introduction of one of the most damaging alien predator, the ship rat (Rattus rattus), on most islands constitutes an amazing conservation paradox. A database gathering information on approximately 300 Western Mediterranean islands was analyzed through generalized linear models to identify the factors likely to influence ship rat presence and to account for how ship rat presence and island characteristics may have driven the presence and abundance of seabirds. Our review showed that few Mediterranean islands remain rat-free. At the regional scale, rat presence was only a limiting factor in the abundance of the smallest seabird, the storm petrel (Hydrobates pelagicus), while the distribution and abundance of the three shearwaters were more influenced by island characteristics. We hypothesized that the long-term persistence of these seabirds may have been facilitated by the various biogeographical contexts of Mediterranean islands, likely to provide intra-island refuges.

Genetic divergence in the small Indian mongoose (Herpestes auropunctatus), a widely distributed invasive species

The combination of founder events, random drift and new selective forces experienced by introduced species typically lowers genetic variation and induces differentiation from the ancestral population. Here, we investigate microsatellite differentiation between introduced and native populations of the small Indian mongoose (Herpestes auropunctatus). Many expectations based on introduction history, such as loss of alleles and relationships among populations, are confirmed. Nevertheless, when applying population assignment methods to our data, we observe a few specimens that are incorrectly assigned and/or appear to have a mixed ancestry, despite estimates of substantial population differentiation. Thus, we suggest that population assignments of individuals should be viewed as tentative and that there should be agreement among different algorithms before assignments are applied in conservation or management. Further, we find no congruence between previously reported morphological differentiation and the sorting of microsatellite variation. Some introduced populations have retained much genetic variation while others have not, irrespective of morphology. Finally, we find alleles from the sympatric grey mongoose (Herpestes edwardsii) in one small Indian mongoose within the native range, suggesting an alternative explanation for morphological differentiation involving a shift in female preferences in allopatry.

Seabird modulations of isotopic nitrogen on islands.

The transport of nutrients by migratory animals across ecosystem boundaries can significantly enrich recipient food webs, thereby shaping the ecosystems’ structure and function. To illustrate the potential role of islands in enabling the transfer of matter across ecosystem boundaries to be gauged, we investigated the influence of seabirds on nitrogen input on islands. Basing our study on four widely differing islands in terms of their biogeography and ecological characteristics, sampled at different spatial and temporal intervals, we analyzed the nitrogen isotopic values of the main terrestrial ecosystem compartments (vascular plants, arthropods, lizards and rodents) and their relationship to seabird values. For each island, the isotopic values of the ecosystem were driven by those of seabirds, which ultimately corresponded to changes in their marine prey. First, terrestrial compartments sampled within seabird colonies were the most enriched in δ15N compared with those collected at various distances outside colonies. Second, isotopic values of the whole terrestrial ecosystems changed over time, reflecting the values of seabirds and their prey, showing a fast turnover throughout the ecosystems. Our results demonstrate that seabird-derived nutrients not only spread across the terrestrial ecosystems and trophic webs, but also modulate their isotopic values locally and temporally on these islands. The wealth of experimental possibilities in insular ecosystems justifies greater use of these model systems to further our understanding of the modalities of trans-boundary nutrient transfers.

The changing pace of insular life: 5000 years of microevolution in the Orkney vole (Microtus arvalis orcadensis).

Island evolution may be expected to involve fast initial morphological divergence followed by stasis. We tested this model using the dental phenotype of modern and ancient common voles (Microtus arvalis), introduced onto the Orkney archipelago (Scotland) from continental Europe some 5000 years ago. First, we investigated phenotypic divergence of Orkney and continental European populations and assessed climatic influences. Second, phenotypic differentiation among Orkney populations was tested against geography, time, and neutral genetic patterns. Finally, we examined evolutionary change along a time series for the Orkney Mainland. Molar gigantism and anterior‐lobe hypertrophy evolved rapidly in Orkney voles following introduction, without any transitional forms detected. Founder events and adaptation appear to explain this initial rapid evolution. Idiosyncrasy in dental features among different island populations of Orkney voles is also likely the result of local founder events following Neolithic translocation around the archipelago. However, against our initial expectations, a second marked phenotypic shift occurred between the 4th and 12th centuries AD, associated with increased pastoral farming and introduction of competitors (mice and rats) and terrestrial predators (foxes and cats). These results indicate that human agency can generate a more complex pattern of morphological evolution than might be expected in island rodents.

Alien Mammals of Europe

Mammals are large, charismatic animals that have a mineralised skeleton that may form long lasting fossils. For these reasons, the level of knowledge on this class, together with other vertebrates, is much higher than for any other animal group. Therefore, the available information on introduction patterns, trends of invasions, and detrimental impacts caused to the environment and to human well-being are more detailed than for other groups covered in the DAISIE project. History of mammal invasions is very long, as anthropogenic introductions of mammals started at least since the beginning of the Neolithic period. Ancient introductions involved wild species commensal of humans (i.e., black rat Rattus rattus and house mouse Mus musculus), anthropophilous (i.e., lesser white-toothed shrew Crocidura suaveolens and wood mouse Apodemus sylvaticus) and domestic species (i.e. species domesticated in the Middle East and gone feral, like the Corsican mouflon Ovis aries). Data on alien mammals have been collected from available global reviews (Long 2003; Mitchell-Jones et al. 1999; Lever 1985), national inventories (Austria: Englisch 2002; Denmark: Baagoe and Jensen 2007; France: Pascal et al. 2006; Germany: Geiter et al. 2002; Ireland: Stokes et al. 2006; Italy: Andreotti et al. 2001; Scalera 2001; Liechtenstein: Broggi 2006; Scandinavian countries: Weidema 2000; Spain: Nogales et al. 2006; Palomo and Gisbert 2002; Switzerland: Wittenberg 2006; the UK: Battersby and Tracking Mammals Partnership 2005; Weijden et al. 2005). Databases available on the internet were also used as a source of information (i.e. for Belgium, the Nordic countries, etc.). Other data have been collected through inputs of the experts of the DAISIE consortium, but also with the valuable support of many experts of the IUCN Invasive Species Specialist Group and of the Group of Experts on Invasive Alien Species of the Council of Europe. Independent experts have verified each record, which included information on taxonomy, native range, vector and pathway of introduction, date of introduction, status of the species, basic information on population size, distribution and impacts. Based on the DAISIE database, in the present chapter we present an overview of the main patterns of mammal invasions in Europe, and analyse the main environmental, social and economic correlates to the arrival and successful establishment.