2013-McLaughlan-How Complete is Our Knowledge of the Ezosystem Invasive Species

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Keywords:Cervus nipponCodium fragileEuropeMillennium ecosystem assessmentOxalis pes-capraeProcambarus clarkii

of invasive species on ecosystem services, the Council of Europe has

the internationalctioning (BIOLIEF,eects a growingchange upon hu-he concern of thee need to evaluatecosystem services

quality of information that can be fed into the decision-makingprocess. A pan-European project, DAISIE, provided in 2009 one ofthe most exhaustive inventories of non-native species in Europe(DAISIE, 2009; www.europe-aliens.org) and their most recentgure for the total number of non-native species is 12,177. TheDAISIE project revealed that we only know the ecological andeconomic impacts of approximately 10% of the invasive species inEurope (Vila et al., 2010). Where impacts on ecosystem services are

* Corresponding author. Tel.: 44 1223 336617; fax: 44 1223 336676.E-mail addresses: [email protected] (C. McLaughlan), [email protected]

(B. Gallardo), [email protected] (D.C. Aldridge).1 Author contributions: CM performed the literature review. CM and BG led the

Contents lists available at

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Acta Oecologica 54 (2014) 119e130writing with signicant contributions from DCA.nutrient cycling) and cultural services. Concerned with the impact Successful prioritisation of resources is dependent on thenotable effects on societal well-being, including human, animal andplant health, the production of foods, fuel and bre, and theregulation of vital processes including climate, water quality, soilsand pollination (Simberloff et al., 2013; Perrings, 2010). The Mil-lennium Ecosystem Assessment (MEA, 2005) identied 11 groupsof ecosystem services that are most vital for humanwell-being andmost affected by ecosystem changes. They include provisioning(e.g. food, timber, bre and fuel), regulating (climate, oods, res,

Biodiversity and Ecosystem Services (IPBES) andconference on invasive species and ecosystem funMar del Plata, Argentina, November 2011) rawareness of the negative effects of biodiversityman well-being. While these initiatives reect tinternational community, they also illustrate ththemanyways inwhich invasive species impact e(Pejchar and Mooney, 2009).Invasive species have numerous multilevel impacts, withthe six strategic biodiversity targets for 2020 (EC, 2011). At an in-ternational level, the upcoming Intergovernmental Platform on1. Introduction1146-609X/$ e see front matter 2013 Elsevier Mashttp://dx.doi.org/10.1016/j.actao.2013.03.005only on the species ecological and economic impacts, but also on the effects related to ecosystem ser-vices. We investigated the quality and extent of baseline data detailing the effects that the top 10 of theworst invasive species in Europe are having on their adopted ecosystems. The results were striking, asthe 10 species showed a wide range of impacts on ecosystem services, a number of which were actuallypositive for ecosystems and humanwell-being. For instance, the bivalve Dreissena polymorpha is a prolicbiofouler of pipes and boats, but it can improve water quality through its ltration of nuisance algae, avaluable effect that is often overlooked. We found that negative effects, particularly economic ones, wereoften assumed rather than quantitatively evidenced; for example, the cost of crop damage by speciessuch as Myocastor coypus and Branta canadensis. In general, the evidence for impacts of these worstinvaders was severely lacking. We conclude that invasive species management requires prioritization,which should be based on informed and quantied assessment of the potential ecological and economiccosts of species (both positive and negative), considered in the proper context of the invader andecosystem. The Millennium Ecosystem Approach provides a useful framework to undertake such pri-oritization from a new perspective combining ecological and societal aspects. However, standardguidelines of evaluation are urgently needed in order to unify denitions, methods and evaluation scores.

2013 Elsevier Masson SAS. All rights reserved.

promoted action including the control of invasive species as one ofReceived 11 October 2012Accepted 11 March 2013Available online 12 April 2013far-ranging effects on fundamental ecosystem services, from the provision of food from that system, tohuman health and wellbeing. For this reason, there is an emerging interest in basing risk assessments notArticle history: Invasive non-native species have complex multilevel impacts on their introduced ecosystems, leading toOriginal article

How complete is our knowledge of theof Europes top 10 invasive species?

C. McLaughlan*,1, B. Gallardo 1, D.C. Aldridge 1

Aquatic Ecology Group, Department of Zoology, University of Cambridge, Downing Stre

a r t i c l e i n f o a b s t r a c tson SAS. All rights reserved.osystem services impacts

ambridge CB2 3EJ, United Kingdom

SciVerse ScienceDirect

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sevier .com/locate/actoec

BelindaHighlight

original aim of the study. This is a coarse measure; however it wasthe best compromise to reduce the number of papers and includeonly those with the highest possibility of containing relevantinformation.

3. Results

In total, the ISI Web of Knowledge provided 26,045 scienticpapers on the 10 species investigated, the three fresh water speciesexhibiting notable coverage in comparison with the rest of thespecies (Fig. 1). After lters were applied, a total of 133 scienticpapers and government/NGO reports were reviewed in order tosummarise the effects that the top 10 invasive species have onecosystem services (Table 1). The total number of papers availableexceeded this; however a number of representative studies werechosen to cover all effects, with a particular focus on review papers.There were a number of species where it was notably difcult to

Oecologica 54 (2014) 119e130concerned, this gure is much lower. Such paucity of data makesprioritisation a challenge and risks the inappropriate allocation ofresources towards management programmes. Furthermore, thereis an increasing realisation that many invasive species can have apositive effect on the functionality of an invaded ecosystem,especially where the invaded system is already heavily degraded(Schlaepfer et al., 2011). Such positive effects must also be balancedagainst impacts when assessing the risks of a particular specieswithin a particular region.

In their review, Vila et al. (2010) identied 10 of the worst Eu-ropean invasive species in terms of ecological and ecosystem ser-vices impacts. The list could be seen as controversial, as many otherspecies may well deserve their position amongst the worst,although it is a fair representation of a range of taxonomic groups(mammals, plants, marine and fresh water organisms), regions oforigin (Americas, Asia, Africa, Europe) and impacts. In this study, webuild on Vila et al.s study to provide a comprehensive review of themain impacts (both negative and positive) of 10 of the worstinvasive species on ecosystem services. We further assessed thequality of baseline data in terms of reliability and geographiccoverage of studies supporting the purported impacts and eco-nomic valuation of costs. In other words, we asked: was an effectnoted in only one study or factsheet or reported multiple times indifferent locations? Were economic as well as ecological effectsquantied, and can costs be extrapolated over different geogra-phies? Were there any positive, as well as negative consequencesfor ecosystems or human well-being? Ultimately, this study aimedto identify knowledge gaps in ecosystem services related in-vestigations, and provide guidelines for future research.

2. Methods

In a review of invasive species in Europe, Vila et al. (2010)identied 10 of the worst European invasive species in terms ofecological and economic impacts. The list included four terrestrial:the Canada goose (Branta canadensis), sika deer (Cervus nippon),coypu (Myocastor coypus) and New Zealand buttercup (Oxalis pes-caprae); three fresh water: the zebra mussel (Dreissena poly-morpha), red swamp craysh (Procambarus clarkii) and brook trout(Salvellinus fontinalis); and three marine organisms: the bay bar-nacle (Balanus improvises), green sea ngers (Codium fragile) andJapanese kelp (Undaria pinnatida).

The provisioning, regulatory and cultural ecosystem servicesimpacts of each of the 10 worst invaders were reviewed. The sub-categories listed in the Millennium Ecosystem Assessment (MEA,2005) were used (1. Provisioning: Fresh Water, Food, Timber,Fibre, Fuel; 2. Regulating: Biological Regulation of Ecosystem ser-vices, Nutrient Cycling, Climate and Air Quality, Human Health,Waste Processing, Regulation of Natural Hazards; 3. Cultural Ser-vices: Cultural and Amenity Services). Data were compiled rst byreference to the DAISIE factsheets (www.europe-aliens.org) andthe IUCNs Invasive Species Specialist Group (www.issg.org). Thiswas followed by a Web of Knowledge search by Latin name (ref-erences up to 15 March 2012). No keywords specifying particularecosystem services were included to avoid missing articles thatdescribe such impacts under a different name. In order to highlightthe number of studies related to ecosystem functioning availablefor a given species, we narrowed the results down to the Envi-ronmental Science/Ecology subject area (as opposed to other un-related areas such as Anatomy, Paleontology or Physiology).Here we assume that this lter will include most papers relating toinvasion ecology, and exclude work on, for example, physiology.We acknowledge the limitations of this use of lters, as somepapers may contain information relevant to ecosystem service

C. McLaughlan et al. / Acta120effects which is not immediately obvious from the title andobtain more than one or two relevant papers. O. pes-caprae, theterrestrial plant, and Balanus improvisus, the marine crustacean,were particularly information-poor (three and two informationsources respectively, including the DAISIE factsheet). Of the 6248papers relating to D. polymorpha, when the lter EnvironmentalSciences/Ecologywas applied, only 35% remained (Fig.1). Similarly,only 10% of the work on P. clarkii (of total 7239 studies) fell into thiscategory (Fig. 1). The other fresh water species, S. fontinalis, had atotal of 7512 papers, with 24% falling into the environmental sci-ences category (Fig. 1). Amongst the terrestrial species, O. pes-caprae only produced 100 studies in total, and B. canadensis hadthe highest number, with 1,224, 57% of which related to environ-ment/ecology (Fig. 1). For marine species the trend was compara-tively low numbers of studies (maximum 889 for U. pinnatida). Inthe case of the bay barnacle, B. improvisus, around 70% of theliterature available does relate in some way to environmental sci-ence or ecology, but as we found, very few of these includedinformation on ecosystem services impacts of invasions.

Informationwas categorized using the 11MillenniumEcosystemAssessment effects on ecosystem services (Tables 1 and 2). Wherethere were sub-categories (for example competition and hybridi-zation, within biological regulation of ecosystem services), thesewere identied and described with sub-headings in the nal table(Table 1). For some categories therewere both positive and negativeeffects of a species, or in several cases only positive effects (e.g.Codium fragile and Undaria pinnatida only had positive effects inthe human health category, with their anti-cancer properties).These were distinguished in Table 1, which contains the details ofeach category for which an effect was noted for each of the 10

Fig. 1. Total number of articles retrieved from ISI web of knowledge when using the

Latin name of 10 of the worst invasive species. In dark grey, studies in the categoryenvironmental sciences and ecology.

Table 1Review of the main impacts of the top 10 worst invasive species on ecosystem services as dened by the Millennium Ecosystem Assessment (MEA, 2005). () and () denotes positive and negative impacts respectively. A fullreference list can be found in Appendix 1.

Species Ecosystem function Ecosystem impact details References

Oxalis pes-caprae Food () Agricultural weed which competes with annual crops, reducing yields. The foliagecan make the hand-picking of olives from the ground difcult.

Marshall (1987)

Biological regulation of ecosystemservices

() The expansion of O. pes-caprae has a detrimental effect on biodiversity: rare plantspecies are susceptible to competitive exclusion. When studied in Greece, its expansionresulted in exclusion of all other species in the understory of olive groves.

Petsikos et al. (2007)

() Possible positive effects of this species include providing honey bee forage andpreventing the establishment of other weeds, leaving soil bare by summer.

DAISIE (2006a)

Nutrient cycling () Net Primary Production was reduced overall by its presence. This is a consequence oflower biomass production and also faster decomposition compared to native plants.This is likely to affect carbon cycling in the ecosystem when O. pes-caprae is present inlarge areas.

Petsikos et al. (2007)

Cultural and amenity services () Much of its European range is valuable for its rare ora and spread of this speciesthreatens ecotourism value of these regions (particularly Mediterranean old elds).

DAISIE (2006a)

Branta canadensis Fresh water () Large amounts of droppings can cause nutrient loading and eutrophication of waterbodies, many of which are used for public recreation. Of their vegetable-based diet, onlyaround 30% of the value of the food they consume is absorbed.

Giles (1992); Banks et al. (2008)

() Lesser Snow geese and Ross geese each found to excrete 3.15 g N/day and 0.45 g P/day, which is a signicant contribution to eutrophication.

Post et al. (1998)

Other literature unsure of the impact bird droppings would have: e.g. concluded mostwould sink to the bottom and have little effect unless major wind event.

Unckless and Makarewicz (2007)

Food () Branta canadensis will feed on crops and there are reports of localised agriculturaldamage. They will eat cereals, root crops and oilseed rape, and grazing pasture land, andwhen large ocks stay at a site for a prolonged period of time they can cause signicantcumulative damage. The species are said to have benetted from an increase in winter-sown cereals, which provide them with a food source in late winter.

Simpson (1991); Watola et al. (1996);Anselin et al. (1996); Banks et al. (2008)


() Hybridisation with native species: Canada geese are known to have hybridised with16 species of Anatidae including Barnacle (Branta leucopsis), Greylag (Anser anser), andEuropean white-fronted (A. albifrons) geese. They are also considered a threat to theGreylag goose (Branta rucollis) in Scotland, through hybridisation and introgression.

Rehsch et al. (2006)

() Displacement of native species: this can be through direct aggression (e.g. they havebeen observed to kill both Moorhen, Gallinula chloropus and Coot, Fulica atra), or drivingnative species numbers down through sheer density (e.g. native geese and divers inNorway), and competition for food.

Fabricius et al. (1974); Banks et al. (2008);Rehsch et al. (2006)

() Damage to wetland habitats: As with agricultural sites, Canada geese can also damagenatural habitats of conservation value. Overgrazing of aquatic and terrestrial plants andtrampling may damage these areas.

Banks et al. (2008)

Nutrient cycling () Changing soil conditions: as with the deposition of faecal matter in water, largeamounts in soil could, on a local scale, alter conditions.

Banks et al. (2008)

Human health () Faeces in public places: lack of research as to whether large amounts of faeces inpublic parks could constitute a danger to humans. Zhou et al. (2004) for example,investigated the prevalence of Cryptosporidium spp. in Canada goose faeces, andconcluded that it could probably play a minor role at most in transmission to humans.

Zhou et al. (2004)

() Aviation safety: Because of their tendency to form ocks and large size, this specieshas been known to have been involved in several strikes with aeroplanes.

Watola et al. (1996)

Cultural and amenity services () The presence of large numbers of this species in amenity areas such as public parkscould reduce the value of these areas through damage to grassy areas from tramplingand faecal matter, eutrophication of amenity water bodies, and the aggressive behaviourof large ocks.

Conover and Chasko (1985)

() In North America, it has been noted that conict between humans and Canada geesehas increased as goose populations have grown.

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Table 1 (continued )


Myocastor coypus Food () Coypu are a known agricultural pest and will eat both winter and summer cropsincluding sugar beet, swedes, kale and cereals.

Norris (1967); Carter and Leonard (2002)

() Coypus are valued as a source of fur and have been used as a meat source.Biological regulation of ecosystemservices

() Their feeding habits mean that in marshland habitat they can be responsible fordestroying large areas of aquatic plants. One example is the Norfolk Broads (UK), whereselective feeding on Phragmites australis opened up the waterways and changed thevegetation composition.

Boorman and Fuller (1981)

() However, until numbers of coypu reach a point at which they become a nuisance,they have often been thought to be useful for aquatic weed control/opening upwaterways and have even been introduced specically for this purpose.

Carter and Leonard (2002)

Human health () The coypu has been shown to be a repository for the parasite Leptospirosis, and couldtherefore contribute to the 1disease in domestic animals.

Carter and Leonard (2002); Waitkins et al. (1985)

Regulation of natural hazards:oods and res

() Burrowing behaviour leads to a serious effect of coypu on ecosystem function: theundermining of river banks and dykes, increasing the threat of ooding.

Norris (1967)

Cultural and amenity services () The destruction of marshland habitat leads to a loss of an ecosystem that is widelyenjoyed recreationally (e.g. the Norfolk Broads in the 50 s/60 s).

Boorman and Fuller (1981)

Dreissena polymorpha Fresh water (/) They are extremely efcient lter feeders and remove algae and microorganismsfrom thewater. Some of themost common (man-made) systems inwhich they occur arereservoirs and water treatment works, where their presence has a direct effect on thewater being supplied to the local population. The effect of the ltration directly on thewater is to increase clarity and therefore improve water quality: this could therefore beseen as a positive effect and this power is being harnessed in several ways in freshwaterhabitats.

Reeders and Bij de Vaate (1990); Macisaac (1996);Higgins and Vander Zanden (2010); Lindahl et al.(2005); Orlova et al. (2004)

() However, there is sometimes increased possibility of cyanobacterial algal blooms,caused by selective feeding pressure by D. polymorpha. Fouling of hard structures oftenaffects water treatment infrastructure, as zebra mussels colonise anything frompipelines to ltration beds.


() Competition with native species: Adverse effects on unionid molluscs throughcompetition for space and food. D. polymorpha will grow directly on unionids andgradually kill them by preventing feeding and eventually causing them to sink into thesediment.

Aldridge et al. (2004); Sousa et al. (2011)

() However D. polymorpha themselves also represent a food source, for somewaterfowl, sh and craysh.

Macisaac (1996)

(/) Ecosystem engineers: D. polymorpha change the benthic habitat throughbiodeposition of organic material (pseudofaeces) and increase the surface area andcomplexity of the habitat with their shells. Some species of invertebrate benet from theincreased habitat/food source created (e.g. gastropods, annelids and amphipods),whereas others show a decrease in diversity or abundance.

Stewart and Haynes (1994); Silver Botts et al. (1996);Nalepa et al. (2003)

() Bioaccumulation of pollutants: D. polymorpha can magnify organochlorine and metalcontaminants through their lter feeding activities. As they can serve as a food sourcefor sh and waterfowl, this could mean transfer of pollutants to higher trophic levels.

Reeders and Bij de Vaate (1992); Mersch and Pihan(1993)

() Changes in zooplankton populations: Zooplankton may be adversely affected eitherdirectly or indirectly by D. polymorpha establishment. Small organisms such as rotifersand protozoans can show declines in population, although it is hard to disentangle theeffects of direct consumption and suppression through competition for food. This mayhave a knock-on effect on food availability for some planktivorous sh.

Macisaac (1996); Higgins and Vander Zanden (2010)

() Shift to a clear water state: A primary effect of this species is their tendency to drivesystems to a clear-water, macrophyte-dominated state by reducing turbidity andallowing macrophytes to grow. Once macrophytes are present again this creates habitatfor benthic invertebrates, and zebra mussel faeces provides food, completing the shiftfrom pelagic to benthic food webs

Strayer et al. (1999); Macisaac (1996)

Nutrient cycling/water processingand detoxication

() D. polymorpha cause major shifts in ecosystem function through selective andefcient feeding on phytoplankton; therefore moving nitrogen and phosphorus fromthe pelagic zone. Several studies have addressed the idea of harnessing this quality in apositive manner for the bioremediation of eutrophic freshwaters.

Goedkoop et al. (2010); Mackie and Wright (1994);Stybel et al. (2009); Antsulevich (1994)

Human health () Cyanobacterial blooms can be a risk to human and animal health Chorus et al. (2000); Briand et al. (2003)

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Cultural and amenity services (/) Large numbers of sharp shells could cause injury and impact on the amenity valueof recreational areas. Cyanobacterial blooms can cause recreational areas to becomeunusable. However, equally zebra mussels could be harnessed to improve water qualityin areas where algal blooms have reduced the aesthetic appeal and biodiversity of awater body. This would apply particularly to man-made reservoirs which are verypopular for activities such as sailing and kayaking.

Chorus et al. (2000); Pretty et al. (2003); Hosper andJagtman (1990); DAISIE (2006b); Brierley and Harper(1999)

Balanus improvisus Biological regulation of ecosystemservices

() This species is a biofouler of other organisms, such as the bivalve Didacna sp. Balanuswill then compete for surrounding food particles.

Riedel et al. (2006)

Human health () There is a risk of sharp shells causing injuries on recreational beaches. DAISIE (2006c)Cervus nippon Food (/) Damage to agricultural crops is reported, for example winter-sown corn and

pasture land. However this is usually minor and localised. Sika deer are also reported todamage crops in their native range in Japan. However stags are also shot for food insome areas, and command high prices.

Long (2003); Onoyama (1990); Prez-Espona et al.(2009); Wittenberg (2005)

() C. nipponTimber, bre, fuel () Consistently suggested as the most serious impact of C. nippon is the damage caused

to commercial forestry. They remove bark, eat the leading and lateral shoots of youngtrees and stags perform bole scoring: a characteristic territory marking by this species.Between 22 and 76% of all newly planted trees had their leading shoots damaged by thedeer.

Long (2003); Lowe (1994), Larner (1987); Carter (1984);Welch et al. (2001); Gill (1992)


() Damage to forest habitat: It is worth noting that sika deer are not reported as causingsignicant damage to areas of conservation concern in the literature reviewed. InIreland it has been suggested that clearings made in the forest make it easier for anotherinvasive species (Rhododendron ponticum) to colonise. Deer can then use the shrub forshelter.

Simberloff and Von Holle (1999); Prez-Espona et al.(2009)

() Hybridisation: Breeding and hybridisation occurs between C. nippon and native deerspecies (red deer: UK), which is a conservation concern.

Corbet and Harris (1991); Prez-Espona et al. (2009);Battersby (2005); Abernethy (1994)

() Competition: Direct competition for food between sika and red deer was reported inthe US.

Armstrong and Harmel (1981)

() Conservation: Decreasing in much of its native range, and populations in othercountries therefore have the potential for conservation value.

Wittenburg (2005)

Human health () Vectors of disease: Aswith all deer species, there is a risk from diseases such as TB andLyme disease, as sika play host to the ticks which act as vectors.

Bohm et al. (2007); Battersby (2005)

() Road hazard: As with other large mammals, these deer could pose a risk for roadsafety if they are involved in collisions.

Wittenberg (2005)

Water processing anddetoxication

() When forest damage applies to watershed protection forests, there is a chance thatthis could interfere with the ability of forest to provide natural water processing anddetoxication as an ecosystem service.

Daniel (1962)

Cultural and amenity services (/) Damage to forestry could impact the amenity value of these forests, as well as thelocal economy. However deer, in general, are economically important to ruralcommunities for shooting, and in some areas sika stags have been commanding higherprices than those of native red deer.

Prez-Espona et al. (2009)

Procambarus clarkii Food (/) Farmed for food, which could be of benet to the local economy, although it isargued that this is very small scale in Europe, and that costs outweigh benets. Risks ofusing this species for commercial operations include physical damage to the habitat,capture of non-target species, and release into the wider area. Rice growing areas areaffected; they make burrows which undermine irrigation structures, and interrupt thegrowth of the crop.

Geiger et al. (2005); Huner (2002); Anastacio et al.(2000)


() Shift in trophic state mediated by macrophyte consumption: P. clarkii is an omnivore,and is often noted to consume macrophytes where it establishes (although someauthors observed selectivity in species of macrophyte chosen). Exclusion experimentshave conrmed this in several cases, and the result is an ecosystem driven towards aphytoplankton-dominated turbid state.

Rodriguez et al. (2003); Rodriguez et al. (2002);Geiger et al. (2005); Cronin (1998)

() Predators of aquatic invertebrates: Juveniles readily feed on invertebrates,particularly from the benthic zone. They show a preference for gastropods andarthropods, and this feeding habit can have a direct effect on invertebrate numbers, andknock-on trophic effects on lower trophic levels.

Hobbs (1993); Gutierrez-Yurrita et al. (1998)

() Competition with native craysh: Has similar habitat and feeding requirements to thenative species it encounters when it invades.

Geiger et al. (2005)

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Table 1 (continued )


() Vectors of disease for native craysh: Carries the infectious oomycete Aphanomycesastaci, which can be deadly for other, native species. P. clarkii has been found to carry themost drought tolerant strain of the diesease. It can also carry the protist diseasePsorospermiasis.

Dieguez-Uribeondo and Soderhall (1993);Dieguez-Uribeondo et al. (1995)

(/) Opening up new trophic pathways: Many large predators (birds, mammals andeven sh) will consume P. clarkii. This reduces the number of trophic levels in anecosystem and opens up new pathways, further altering ecosystem dynamics. However,P. clarkii also provides a food resource to higher predators, and has been shown to behaving positive effects on several birds of high conservation value.

Correia (2001); Tablado et al. (2010)

() Bioaccumulation of heavy metals: Craysh captured inside contaminated areasaffected by toxic spills been shown to have a higher heavy metal content than thoseoutside. They can be used as biological indicators of heavymetal pollution. They are ableto immobilise the metals in their tissues, but these are then ingested by predators,presenting a risk of biomagnication. Further studies of effects on vertebrates needed.

Geiger et al. (2005); Daz-Mayans et al. (1986);Suarez-Serrano et al. (2010)

Nutrient cycling () Benthic lter feeding disturbs the sediment and causes bioturbation. This leads tonutrient release. However, it is difcult to distinguish increases in nutrient levels causedby P. clarkii invasion and by other factors (such as increased fertiliser use). Some studiesfound the signicance of changes in nutrient levels to be insignicant at an ecosystemlevel.

Rodriguez et al. (2003); Angeler et al. (2001)

Human health () There is still a question over whether craysh could be signicant vectors for humandiseases. However, a recent outbreak of tulermia in Spain was related to P. clarkii.

Anda et al. (2001); Geiger et al. (2005)Vasconcelos et al. (2001); Tricarico et al. (2008)

() P. clarkii is known to feed on surface microalga, including toxin strains ofcyanobacteria such as Microcystis aeruginosa, and can bioaccumulate the toxins in itstissues. However most of the toxin was found in the intestine and hepatopancreas, sorisk to human health may be minimal if these parts are removed. Bioaccumulation upthe food chain remains an issue.

Cultural and amenity services () Although it has been suggested that commercial production of P. clarkii for food isonly on a small scale in Europe, shing can also be a recreational activity, which couldbring economic value.

Geiger et al. (2005)

Undaria pinnatida Biological regulation of ecosystemservices

() Changes in species assemblages: By increasing habitat complexity, it increases therichness and abundance of crustaceans, urchins, nemertines and polychaetes. It hasbeen suggested that Undaria could potentially produce a bottom-up effect on local foodchains by increasing abundance of prey for a wide variety of predators, frominvertebrates to marine mammals.

Casas et al. (2004); Irigoyen et al. (2011a, 2011b)

() However, it is also known to reduce native seaweed diversity and reduce the habitatfor reef shes by physically obstructing their refuges.Food web impacts: It impedes light penetration under it with important bottom-upeffects. When it dies it forces sh and other animals to move to nearby areas(/) Bioaccumulation of pollutants: It can absorb Hg, Cd and Ni. This ability has beenused in Japan to track the geographic distribution of metals in coastal waters usingUndaria as a bioindicator. Metals can be transferred to higher order consumers,including humans.

Seki and Suzuki (1995); Yamada et al., 2007

Ecosystem engineer: U. pinnatida occurs in dense stands being able to grow 1e2 cm perday, forming a thick canopy down to 15 m in clear waters.

Timber, bre, food () Commercially cultivated for its high nutritional values (high in iodine, salt, fatty acidsand fucoxanthins), anti-oxidant and anti-obesity properties

Casas et al. (2004); Maeda et al. (2005)

() It can negatively affect the commerce of other native algae. For example, Undaria hasrecently been found in populations of the agar-producing red alga Gracilaria gracilis nearNuevo Gulf (Argentina).() Fouling of marine-culture facilities (n sh cages, oyster racks, scallop bags andmussel ropes). Heavy fouling may also restrict water ow through cages. Undaria canpotentially foul mussel farms, salmon farms and boats. Heavy infestations of Undariamay also clog marine farming machinery, slow growth of mussels and restrict watercirculation. Heavy fouling of boats seriously decreases their efciency. Efforts arecurrently being made to avoid its dispersal into commercial shellsh beds in Argentina

Casas et al. (2004)

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Human health () Its extracts can be used to develop antitumour, anti-viral (sulphated polyanions),against herpes, anti-osteoporotic, anti-hypertension, and insulin resistance medicines,as well as to reduce erythema (methanol). However this is rather a potential economicbenet rather than a real human health impact

Hayasi et al. (2008); Lee et al. (2004); Maruyama et al.(2003); Suetsuna et al. (2004); Vishchuk et al. (2011)

Codium fragile Biological regulation of ecosystemservices

() Changes in species assemblages: By increasing habitat complexity, increase inabundance and diversity of macroinvertebrates like amphipods, harpacticoids, slugs,nematodes and bivalves. Provides anti-predation refuge to scallops. Enhances thecolonization by mussels. It has been associated with greater abundances of shes asApeltes quadracus and Tautogogolabrus adspersus in eastern Canada.

Chavanich and Harris (2004); Drouin et al. (2010, 2011,2012), Kelly et al. (2011); Sumi and Scheibling (2005);Trowbridge (2001); Watanabe et al. (2010)

() Displacement of native kelps (e.g. C. tomentosum, Laminaria longicrucis andL. digitata), sea urchins, lobsters, oysters, eels and marine plants.() Ecosystem engineer: forms dense stands impeding the movement of animals andincreasing sedimentation rates. Fouling of shellsh beds. Colonizes eelgrass beds(Zotera) by epiphytically attaching to its rhizomes potentially disturbing these coastalecosystems through competition and disturbance. Increases shading potentiallyaffecting other algae. Alters the dynamics of detrital subsidy from high to lowproductivity areas through changes in quantity and nutritional quality of detritalmaterial: C. fragile degrades slower and has a lower C/N ratio than native kelp Saccarinalattisima in Nova Scotia (Canada).

Bulleri et al. (2005, 2006); Harris et al. (2001);Krumhansl and Scheibling (2012); Scheibling andGagnon (2006)

New products/industries frombiodiversity/human health

() Derivatives from this species (siphonaxanthin) can be used to supress cancer.Galactant derivatives have immunostimulating effects via activation of macrophages.Also antiviral and anticoagulant effects.

Ganesan et al. (2010); Jurd et al. (1995); Kim et al.(2008); Lee et al. (2010)

Timber, bre, food () Very high nutritious potential as diet complement or animal feeding. Extensivelyfarmed in Korea and other South-East Asia countries.

Hwang et al. (2008); Ortiz et al. (2009)

Water processing anddetoxication

() High potential to use for bioremediation (reduce nutrient loads, overall inorganicnitrogen) due to its year round rapid growth.

Hanisak and Harlin (1978); Head and Carpenter (1975);Kang et al. (2008)

Cultural and amenity services () Overgrows in sheltered parts of ports (wharf pilings, jetties, ropes), where it benetsfrom the high nutrient loads and human-assisted dispersal

ISSG

() Fouls port facilities and shing gear. Rotting ashore can affect tourismSalvelinus fontinalis Biological regulation of ecosystem

services() Hybridization with native species (S. conuentus, S. malma, Salmo trutta) reducesgenetic diversity and threatens the conservation of species.

DAISIE (2006d); Marie et al. (2010, 2012); Webster andFlick (1981)

() Predates and displaces native sh species (e.g. Salmo trutta, Oncorhynchus aguabonita,O. clarki, O. henshawi, O. tshawytsch, S. conuentus and other salmonids). Also predateson amphibians, zooplankton and other invertebrates, changing their composition andabundance.

Drouin et al. (2009); Dunham et al. (2002); Fausch andWhite (1981); Korsu et al. (2009); Llewellyn (2011);Macneale et al. (2010); Magnan (1988); Rieman et al.(2006); Spens et al. (2007)

() Unlike native trout, its not a suitable host for endangered unionid Margaritiferamargaritifera. When introduced to shless lakes, it can threaten endangered frogs (Ranachiricahuensis, Pseudacris maculate, P. regilla, R. luteiventris, R. sylvatica, R. cascadae,R. iberica, R. muscosa and Ascaphus truel), salamanders (Ambystoma tigrinum, A. gracileand A. macrodactylum), toads (Bufo boreas) and newts (Triturus marmoratus)

Parker and Schindler (2006)

() Food web changes: alters nutrient cycles in oligotrophic lakes by re-suspendingphosphorus from lake sediments and stimulating primary productivity. The biomass ofsmall insects (e.g. Chironomidae) are favoured is higher when S. fontinalis is present,whereas the biomass of large insects (e.g. Ephemeroptera) is reduced.

Bechara et al. (1992); Cucherousset et al. (2007);Magnan (1988)

Cultural and amenity services (/) Important sport shing species although it is also negative if salmonids disappear. DAISIE (2006d)

C.McLaughlan

etal./

Acta

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54(2014)

119e130

125

dingsed

OecTable 2Summary of the impacts of the 10 worst invasive species on ecosystem services accorLight grey reects mixed positive and negative impacts. The diagonal patterning is u

Fres

h W

ater

Food

Tim

ber,

Fibr

e, F

uel

ew P

rodu

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tries

from

Biod

iversi

ty

C. McLaughlan et al. / Acta126species. By way of example, D. polymorpha affects nutrient cyclingmostly through selective feeding on phytoplankton, thereforemoving nitrogen and phosphorus from the pelagic zone to thebenthos (Goedkoop et al., 2011). The 10 species had wide-rangingeffects across the categories of ecosystem services (Table 2), witha minimum of two out of eleven affected (S. fontinalis andB. improvisus) and a maximum of six (B. canadensis, M. coypus,D. polymorpha and C. nippon). Only one category (climate and airquality) did not seem tobe affected byanyof the 10 species (Table 2).In contrast, biological regulation of ecosystem services appeared forevery species (Table 2).

In general, there seemed to be a knowledge gap as far as eco-nomic effects were concerned, especially when considering thesame species effects in different regions. Effects on ecosystemssuch as nutrient cycling and ecosystem engineering were wellcovered in papers, and genetic studies on hybridization werewidespread. Positive and negative effects for the same species wererarely presented together in an integrated fashion.

N

Oxalis pes-caprae

Branta canadensis

Myocastor coypus

Dreissena polymorpha

Balanus improvisus

Cervus nippon

Procambarus clarkii

Salvelinus fontinalis

Codium fragile

Undaria pinnatifida to the literature available for each species. Dark grey denotes negative impacts only.when only positive impacts are reported in the literature.

olog

ical

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of Ec

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em Se

rvice

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Nutr

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Cyc

ling

Clim

ate

and

Air Q

uality

Hum

an H

ealth

Wat

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s

ologica 54 (2014) 119e1304. Discussion

Good quality data which can be used to form a consensus on thetype and severity of effects an invasive species has is essential formanagement decisions. A huge body of work exists on invasivespecies, and 10 of the worst species in Europe are no exception tothis. However the results of this study suggest a surprisingly smallproportion of papers relate to ecosystem services and humanwellbeing. Most of the evidence of such impacts is currently in theform of government reports, which often rely on expert consulta-tion and generally extrapolate the ecological and economic costs ofinvaders across broad geographies. While extrapolation can beuseful and necessary, particularly when used as an early warningfor prevention in another location, risk assessments should eval-uate potential impacts considered in the proper context of thespecies and ecosystem invaded. Economic effects are well studiedin the case of some species (e.g. D. polymorpha), but much less so inothers.While the preferred response to established invasive species

Bi

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Oecowill often be eradication, resources are limited and thus clearermethods of prioritization would help identify those species withmore negative effects than others, and therefore in more need ofurgent action.

4.1. Terrestrial organisms

The four terrestrial species comprised one plant, a large speciesof waterfowl, a semi-aquatic rodent and a deer. The plant, O. pes-caprae, was one of several species which was extremely lacking inevidence to support some of the purported impacts. A negativeeffect on biodiversity and ecotourism inMediterranean Old Fields ispresumed in the DAISIE factsheet (DAISIE, 2006a) from studieswhich show competitive exclusion (Marshall, 1987), however nowork could be found actually quantifying effects on ecotourism.Other identied impacts were those that might be expected froman invasive plant: reduction of crop yields (Marshall, 1987) andchanges in nutrient cycling (Petsikos et al., 2007). Positive effectssuch as providing honey bee forage were mentioned, but not evi-denced outside of the DAISIE factsheet and we could not ndsupporting data.

Several themes can be identied in the impacts of the threeterrestrial vertebrates. These large species are highly likely to causetheir main negative effects through direct damage, either to a cropfor food or timber (food crops in the case of B. canadensis andM. coypus and commercial forests in the case of C. nippon) orphysical damage to habitats, with concomitant consequences forother organisms, reduction in aesthetic appeal and even increasedrisk of natural disasters, such as oods (Norris, 1967). This bringsthem often into direct conict with humans. All three species arevectors or possible vectors of disease. C. nippon is a likely vector forany tick-borne disease such as Lyme disease (Bohm et al., 2007).Although this role can be also played by native deer populations,the presence of C. nippon could increase the available hosts for theparasite. A prominent theme under the biological regulation ofecosystem services category is hybridization. Both C. nippon andB. canadensis are known to hybridise with native species (Corbetand Harris, 1991; Rehsch et al., 2006), and this is of serious con-servation concern. We found surprisingly little quantication ofeconomic costs from the activities of these species, which suggeststhey may be understudied and/or difcult to quantify. One eco-nomic positive was nevertheless noted in the case of C. nippon: thehigh prices that are increasingly commanded for C. nippon stags inhunts (Prez-Espona et al., 2009).

4.2. Fresh water organisms

Fresh water invasives can undoubtedly have potentiallyextremely serious effects. Consequently, a standout theme for thethree species reviewed here was the impact on native species andthe transformation of the physical structure and general trophicfunctioning of habitats. The bivalve, sh and craysh all displacenative species, through competition for food and space, trans-mission of disease, predation and biofouling (e.g. Aldridge et al.,2004; Geiger et al., 2005; Korsu et al., 2010). D. polymorpha andP. clarkii are bioaccumulators of metals and organic compounds(Reeders and Bij de Vaate, 1992; Geiger et al., 2005). All three alsohave signicant effects on food webs and the character of habitats,for example P. clarkii consumes macrophytes and certain benthicinvertebrates (Hobbs, 1993), D. polymorpha deposits shells andfaeces (Stewart and Haynes, 1994; Sousa et al., 2009), andS. fontinalis stimulates primary productivity by re-suspendingphosphorus from lake sediments (DAISIE, 2006d). Changes in wa-ter chemistry and water processes in general are a predictable

C. McLaughlan et al. / Actaresult of aquatic invasions. All of these species have some effect onnutrient levels/nutrient cycling. However as an extremely efcientalgal lter feeder, D. polymorpha has perhaps the most signicanteffects on water processes. It can cause a shift from a turbid to aclear water state, with signicant consequences for nutrient richwater bodies which it inhabits (Macisaac, 1996). Most change inthis context is automatically seen to be negative, and positive ef-fects e in this case water quality improvements related to thepresence of lter feeders e are generally overlooked, particularlypositive economic effects (Elliott et al., 2008; Pysek et al., 2008;Schlaepfer et al., 2011). For some species, and indeed some regionsof the world, economic impacts are well-understood and quanti-ed; for example, zebra mussels, as well as other invasives, in theUS (Nalepa and Schloesser, 1993; Lovell and Stone, 2005; Pimentelet al., 2005) and Europe (Oreska and Aldridge, 2011). Howevercosts often include eradication costs, not just direct costs to otherindustries (e.g. Pimentel et al., 2005), and by not accounting forpositive economic impacts (Stybel et al., 2009; Ewel et al., 1999),only one side of the story is considered. Acknowledging such pos-itive economic outcomes is obviously dangerous, as it can triggerthe protection, encouragement and even intentional introductionof the invader (Nuez et al., 2012). However, we cannot ignore thefact that many invasive species, and sometimes the most prob-lematic ones, have a clear economic value that makes their controland eradication certainly difcult, sometimes even impracticable.This is the case of many introduced shes (including one of ourstudy species, S. fontinalis) whose management is thoroughlyopposed by local anglers and sherman. By way of example, after asuccessful, and presumably costly, campaign to eradicate theinvasive northern pike (Esox lucius) in Lake Davis (California, US),locals are believed to have intentionally reintroduced it to promoteshing (Elmendorf et al., 2005). This reects the inability of re-searchers and environmental managers to communicate on theissue of invasive species, and suggests new strategies engaging allrelevant players are needed to manage biological invasionsconsidered in their socio-economic context. In this sense, not onlythe direct costs for industry or governments, but the ecosystemservices impact also needs to be quantied. Lack of a proper eval-uation of the costs of invasive species impedes the comparison ofspecies and hampers the investment of governments in the pre-vention and control of species.

4.3. Marine organisms

Two species of algae and a crustacean made up the marinecontingent of the top 10 invasive species. A feature all three have incommon is their potential as biofoulers, be it on port facilities,commercial shellsh operations or other organisms. ForU. pinnatida and C. fragile this can mean economic consequences,as they slow down growth on mussel farms, or clog harvestingmachinery (Casas et al., 2004; ISSG www.issg.org). Notably,B. improvisus was extremely lacking in the literature search andtherefore a full review of its effects may not have been made. Thesuggestion that it could cause injuries if the shells were numerouson beaches, for example, seems to be a supposed andminor impact,with no quantitative evidence available. U. pinnatida and C. fragileinevitably cause similar impacts to one another. Both can un-doubtedly have negative effects on native species assemblages, bydisplacement of other algae, sh and invertebrates, and also byforming dense stands which impede light penetration and causeimportant top-down effects (Bulleri et al., 2006). In some casesthere is a lack of evidence or at least relevant evidence from arecent timescale or the same continent. C. fragile, for instance, isreported to be damaging to the aquaculture industry, and in Canadaeconomic losses have been valued at $1.2 million USD per year

logica 54 (2014) 119e130 127(Colautti et al., 2006). However in Chile, where it is now well

Oecestablished, much less is known about its ecology and economiceffects (Neill et al., 2006). Perhaps surprisingly, both species alsohad a number of notable positive effects. One of these, not noted forany of the previous eight invasive species, was the potential to haveimportant applications for human health. Both have several med-ical applications including anti-cancer properties (Vishchuk et al.,2011; Ganesan et al., 2010). However, this does not serve as anargument to allow them to proliferate unchecked outside of theirnative range. Both also have value as high-nutrient human/animalfood (Ortiz et al., 2009; Casas et al., 2004). In common withD. polymorpha, C. fragile has been suggested as having highpotential as a bioremediator to reduce nutrient loading (Kang et al.,2008).

4.4. Positive effects of invasive species on ecosystem services

The study of the positive effects of invasive species is receivingincreasing attention (see Schlaepfer et al., 2012). It has been sug-gested that although most invasion ecologists try to remainobjective, there is a persistent bias against invasive species in theliterature, for example in the topics chosen for study and the as-sumptions made about invasive species values (Gurevitch andPadilla, 2001; Sagoff, 2005). The importance of placing non-nativespecies in the proper context was highlighted by Davis et al.(2011). They stated that emotive reasoning is often used when itcomes to management of non-natives. Invasive species positiveeffects will inevitably be neglected or diminished by researcherswhose main objective is to raise awareness and justify their pre-vention and control. This is a point of view which is controversialwith many invasion ecologists (see Simberloff, 2011). However theoverarching message about prioritization in a reality where moneyis limiting is an important one. Schlaepfer et al. (2010) attempted tocatalogue the ways in which non-native species can contribute toachieving conservation goals. While fully acknowledging thenegative aspects of the species, the authors found several methodsby which non-natives were contributing to conservation, such asproviding shelter and food for native species, acting as ecosystemengineers and boosting ecosystem services such as pollination andbioltration. Invasive species could also be replacing importantfunctions in ecosystems where the original provider is long sincelost, likely as a result of habitat change or pollution rather than theinvasion itself. A good example of this is in the case of ecologicalrestoration, where invasive plants can provide functions such asacting as nurse plants, seed recruitment and provision of fuelwhere burning is part of the ecology (Ewel and Putz, 2004). Non-native animals can also provide the functions of their extinct orrare native cousins, e.g. the Aldabra giant tortoise (Aldabrachelysgigantea) replaces the ecological role of extinct giant Cylindraspistortoises in the Mascarene Islands (Grifths and Harris, 2010). Wetherefore need a better evaluation of positive and negative effectsof species on ecosystem services in order to inform their manage-ment, and support prioritization. Of course, prevention of invasionswill always be the preferred option, and we do not suggest thatinvasions are facilitated in order to benet from any positive effects.As Simberloff et al. (2013) emphasize, good control measures, suchas the biocontrols in place at New Zealands borders, can be ef-cient and, in the long term, far more cost effective than latermeasures once a species is released.

4.5. Towards an ecosystem services oriented scoring system forinvasive species

There exist a large range of threat-scoring systems in the liter-ature that aim to achieve a thorough assessment of species and

C. McLaughlan et al. / Acta128habitats (e.g. Catford et al., 2012; Molnar et al., 2008; Nentwig et al.,2010). In their proposal to assess marine invasions, Molnar et al.(2008) scored species considering four important categories:ecological impact, geographic extent, invasive potential (spread)and management difculty. Within these categories, the species isgiven a numbered score dependent on the severity of the effect (forexample in geographic extent a score of 1 would mean a singlesite, and 4 would be multi-ecoregion spread). Interestingly, whenevaluating the ecological impact, emphasis is made on theecosystem processes affected by the invader. In the case of Nentwiget al. (2010), two main categories of impacts are considered:environmental (e.g. competition, predation, hybridization) andeconomic (e.g. on agriculture, livestock, forestry). For both cate-gories, scores are given to species from 1: little disruption, to 4/5:multiple severe impacts, including U/0: no or little information todetermine score. Although the two scoring systems can give indi-rect indication of ecosystem services impacts, we suggest adding acategory of functional impacts where scores are assigned for eachspecies considering the ecosystem services impacted, as proposedby the Millennium Ecosystem Approach (listed in Table 2).Although clear scoring systems such as these could provide a usefulframework, context-dependency for different ecosystems will al-ways need to be considered. For example, the positive effects of thezebra mussel at a drinking water reservoir may outweigh thenegatives, whereas in a stream rich with native unionids this isunlikely to be the case.

4.6. Concluding remarks

In this study we have evaluated the impacts of the 10 worstEuropean invasive species on fundamental ecosystem services andidentied deciencies in the current state of evaluation of species.The 10 species investigated here were selected because they aresuspected to have the highest number of impacts on a dened set ofecosystem services. However, the services are not all equally rele-vant or equally weighted. For example, regulating services en-compasses a huge range of effects on erosion regimes, waterregulation, the spread of disease and many others, whereas cul-tural services often includes minor aesthetic issues, which are alsovery subjective. A species could also be having certain effects to amuch greater or lesser extent in different localities or differentcountries it invades. Because invasive species impacts are context-dependent, prioritization actions must be site-specic, andinvasions should therefore be viewed from the ecosystem level, andnot the species level (Simberloff et al., 2013).

Other species than those evaluated in this study may welldeserve their place amongst the top 10 worst invaders, and wequestion the validity of using these 10 species, in terms of theirproven impacts. For instance, the Asian tiger mosquito Aedesalbopictus is a species which although currently not widelydistributed, poses a serious threat to human health throughtransmission of tropical diseases in Europe (Enserink, 2007). Thespread of this species may be especially facilitated by climatechange. The pine processionary moth (Thaumetopoea pytiocampa)is undergoing a rapid latitudinal and altitudinal expansion from itsnative range in southern France, apparently related to increasingwinter temperatures (Battisti et al., 2005). This pest feeds onseveral Mediterranean Pinus species, such as P. nigra, P. brutia andP. halepensis, inicting serious economic and ecological losses(Hdar et al., 2003), and produces urticating hairs affecting therecreational value of forests it invades. There are also notable ma-rine plants which may well be more harmful than U. pinnatida orC. fragile, for example Carpobrotus edulis, which forms dense matsand aggressively competes with native species (DAISIE, 2006e).

In this study we have noted that invasive species can sometimes

ologica 54 (2014) 119e130have positive impacts via bioltration, pollination, ecosystem

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Supplementary data related to this article can be found online at

zebra mussel (Dreissena polymorpha) in Great Britain. Biological Conservation

green alga, Codium fragile ssp tomentosoides, on recruitment and survival ofmussels. Marine Biology 148 (6), 1213e1220.

OecoCasas, G., Scrosati, R., Piriz, L., 2004. The invasive kelp Undaria pinnatida (Phaeo-phyceae, Laminariales) reduces native seaweed diversity in Nuevo Gulf (Pata-gonia, Argentina). Biological Invasions 4, 411e416.

Catford, J.A., Vesk, P.A., Richardson, D.M., Pysek, P., 2012. Quantifying levels ofbiological invasion: towards the objective classication of invaded and invasibleecosystems. Global Change Biology 18, 44e62.

Colautti, R.I., Bailey, S.A., van Overdijk, C.D.A., Amundsen, K., MacIsaac, H.J., 2006.Characterised and projected costs of nonindigenous species in Canada. Bio-logical Invasions 8, 45e59.

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DAISIE, 2006d. Salvelinus fontinalis Species Factsheet. Available at: http://www.europe-aliens.org/speciesFactsheet.do?speciesId53469.

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DAISIE, 2009. Handbook of Alien Species in Europe. Springer, Knoxville, TN, USA.Davis, M.A., Chew, M.K., Hobbs, R.J., Lugo, A.E., Ewel, J.J., Vermeij, G.J., Brown, J.H.,

et al., 2011. Dont judge species on their origins. Nature 474, 153e154.EC, 2011. EU Biodiversity Strategy to 2020, Brussels (Belgium).Elliott, P., Aldridge, D.C., Moggridge, G.D., 2008. Zebra mussel ltration and its

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and Fishing in Lake Davis. Flag in the Ground Productions, Davis, California, USA.119, 253e261.Battisti, A., Stastny, M., Netherer, S., Robinet, C., Schopf, A., Roques, A., Larsson, S.,

2005. Expansion of geographic range in the pine processionary moth caused byincreased winter temperatures. Ecological Applications 15, 2084e2096.

Bohm, M., White, P.C.L., Chambers, J., Smith, L., Hutchings, M.R., 2007. Wild deer as asource of infection for livestock and humans in the UK. Veterinary Journal 174,260e276.

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Acknowledgements

Funding for the PhD work of C.M. comes from a NERC CASEStudentship, grant code NE/H018697/1. B.G. has received fundingfrom the European Commission (FP7/2007-2013, Marie Curie IEFprogram) under grant agreement n251785.

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C. McLaughlan et al. / Acta Oecologica 54 (2014) 119e130130

How complete is our knowledge of the ecosystem services impacts of Europe's top 10 invasive species?1. Introduction2. Methods3. Results4. Discussion4.1. Terrestrial organisms4.2. Fresh water organisms4.3. Marine organisms4.4. Positive effects of invasive species on ecosystem services4.5. Towards an ecosystem services oriented scoring system for invasive species4.6. Concluding remarks

AcknowledgementsAppendix A. Supplementary dataReferences

2013-McLaughlan-How Complete is Our Knowledge of the Ezosystem Invasive Species

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