THE$IMPACT$OF$INVASIVE$ALIEN$SPECIES$ ON$NATIVE$THREATENED$SPECIES$IN$ EUROPE$ ! Piero!Genovesi,!Lucilla!Carnevali,!Riccardo!Scalera! !
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! THE IMPACT OF INVASIVE ALIEN SPECIES ON NATIVE THREATENED SPECIES IN EUROPE ! ! Authors:! Piero!Genovesi! ISPRA,!Via!V.!Brancati!48,!00144!Rome,!Italy!
Chair!IUCN!SSC!Invasive!Species!Specialist!Group!
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! Lucilla!Carnevali! ISPRA,!Via!V.!Brancati!48,!00144!Rome,!Italy!
IUCN!SSC!Invasive!Species!Specialist!Group!
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! Riccardo!Scalera! IUCN!SSC!Invasive!Species!Specialist!Group!
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Recommended$$ Genovesi!P,!Carnevali!L,!Scalera!R!(2015).!The!impact!of!invasive!alien!species!on! citation:! native!threatened!species!in!Europe.!ISPRA!M!ISSG,!Rome.!Technical!report!for!the! $ European!Commission.!Pp.!18.! Cover$photo:!! Japanese!knotweed!(Fallopia'japonica)!©!Riccardo!Scalera! !
! Summary ! ! Introduction!...... !1! Methods!...... !2! Results!and!discussion!...... !3! Conclusions!...... !13! References!...... !15! Annex!1!M!Complete!list!of!alien!invasive!species!and!groups!that!affect!threatened!(IUCN!Red!List!CR,!! EN,!VU)!species!in!Europe!...... !17!
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Introduction !
Invasive! alien! species! (IAS)! are! considered! the! The!scope!of!the!present!report!is!to!provide!an! second! greatest! threat! to! biodiversity! globally,! assessment! of! the! impact! caused! by! IAS! on! second! only! to! habitat! loss! and! fragmentation! European!biodiversity.!The!objective!is!to!define! (MA!2005).!Besides!being!one!of!the!first!cause!of! a! baseline! against! which! to! measure! the! impact! animal! extinctions! (Clavero! &! GarciaMBerthou! of! the! response! actions! implemented! in! Europe! 2005),! IAS! also! severely! affect! the! ecosystem! to!deal!with!IAS!over!the!next!five!years,!with!a! services! we! depend! upon! (Vilà! et' al.! 2010).! The! special! focus! on! the! measures! directly! linked! to! economic! consequences! of! biological! invasions! the!implementation!of!the!EU!Regulation!on!IAS.! are! also! impressive.! In! Europe! alone! it! is! The! innovative! element! of! this! approach! lies! on! estimated! that! the! overall! losses! due! to! this! the! opportunity! to! base! the! assessment! on! the! threat! are! above! 12! billion! euro/year! (Kettunen! best!available!information!from!key!regional!and! et' al.! 2009).! Furthermore,! there! are! evidences! global!datasets!built!through!the!collaboration!of! showing! that! the! number! of! IAS! in! Europe! is! the!most!reliable!experts!in!the!field.!! constantly! increasing,! with! a! rate! of! 76%! in! the! Given!the!focus!on!a!wide!range!of!species!native! 1970M2007!period!(Butchart!et'al.!2010).!! to! Europe,! this! approach! can! offer! a! The! pressure! of! IAS! is! expected! to! be! steadily! complementary! view! of! the! overall! situation! increasing! over! the! next! decade! if! significant! compared! to! the! two! recent! reports! on! “The! actions! are! not! implemented! (GBO! 4).! To! State! of! Nature! in! the! European! Union”! adequately! address! this! problem,! Europe! has! (European! Commission,! 2015)! and! “State! of! been! developing! a! number! of! tools! over! the! nature! in! the! EU”! (EEA,! 2015).! In! fact! the! data! years.!For!example,!in!2003!the!Bern!Convention! analysed!within!the!present!report!focus!on!the! adopted!the!European!Strategy!on!IAS!(Genovesi! species! “threatened”! (i.e.! within! the! IUCN! Red! &! Shine! 2004),! on! the! basis! of! which! the! List),! while! those! of! the! mentioned! EC! and! EEA! European! Union! (EU)! has! been! working! to! reports!focus!on!species!“protected”!(i.e.!by!the! develop!a!dedicated!policy!and!legislation!on!the! Birds! and! Habitats! directives).! Also! the! issue.! This! work! eventually! resulted! in! the! geographic! scope! is! slightly! different,! as! the! adoption! of! the! EU! Regulation! No! 1143/2014,! present!report!analyses!the!situation!in!the!entire! which! entered! into! force! on! 1st! January! 2015! European! region,! while! the! EC! and! EEA! reports! (herewith! referred! to! as! the! EU! Regulation! on! are! based! on! the! data! available! from! the! IAS).!! monitoring! activities! carried! out! within! the! EU! Member!States.!
! 1! Methods !
The! assessment! is! based! on! the! analysis! of! the! • Category!of!threat!(for!details!see!criteria! data! available! from! two! key! IUCN! knowledge! in!the!www.iucnredlist.org1)! tools:! the! Global! Invasive! Species! Database! (GISD)! M! implemented! by! the! IUCN! SSC! Invasive! • Name!of!the!alien!species!posing!a!threat! Species!Specialist!Group!M!and!the!IUCN!Red!List! (one!record!for!each!alien!species)! of!Threatened!Species.!The!analyses!were!carried! • Impact! mechanism! (of! the! alien! species! out! using! the! onMline! version! of! the! two! tools,! toward!the!red!listed!species)! integrated!with!data!from!the!datasets!available! offMline.!! • Effect!of!impact!on!the!red!listed!species! (outcome)! The! dataset! for! the! present! work! was! built! by! selecting! all! available! data! and! information! on! • Level!of!impact!! native!species!assessed!as!threatened!within!the! IUCN! Red! List! and! reported! as! affected! by! Regarding! the! level! of! impact,! the! following! invasive! alien! species! (Red! List! threat! code! 8.1,! information! is! reported! in! the! dataset:! high,! under! the! more! general! “invasive' and' other' medium,! low,! problematic'species'and'genes”!category).!To!this! no/negligible/unknown/future/past.! The! level! purpose,! all! relevant! data! available! in! the! “high”! is! assigned! whenever! IAS! are! the! only! database!of!the!IUCN!Red!List!under!the!relevant! recognised! threat! for! the! target! species! in! the! code! were! duly! screened,! including! any! IUCN!Red!List,!or!whenever!the!occurrence!of!IAS! additional! information! reported! in! the! narrative! is! specifically! reported! as! the! main! threat.! The! (taking!note!of!additional!details!on!IAS!involved,! level! “medium”! means! that! IAS! are! associated! level!of!threat,!type!of!impacts,!etc.).!! with!other!threats,!while! a! “low”! level! indicates! that!at!least!three!or!more!different!threats!are! As! a! result,! for! each! IUCN! Red! List! assessed! known! to! affect! the! target! species! of! the! IUCN! species,! all! relevant! information! has! been! Red! List.! “Future! threat”! is! assigned! to! an! excerpted!and!included!in!a!dedicated!database.! invasive! alien! species! expected! to! become! a! The!dataset!has!been!further!integrated!with!the! threat! in! the! near! future,! and! “past! threat”! data! excerpted! from! GISD.! In! particular,! for! whenever!an!alien!species!was!recognised!within! impact! mechanisms! and! relevant! effects! the!IUCN!Red!List!as!a!threat!in!the!past,!but!has! (outcomes),!the!classification!schemes!developed! been!currently!removed/mitigated.! within!the!GISD!have!been!used.!Also!information! on! the! level! of! impact! has! been! included! in! the! database,! based! on! the! information! provided! in! the!IUCN!Red!List!assessments.!!
The!key!records!used!for!the!present!analysis!are! the!following:!
• Name!of!red!listed!species!(one!or!more! record! for! each! red! listed! species,! depending! on! the! number! of! alien! !!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!! 1! species!reported!as!a!threat)! http://www.iucnredlist.org/documents/RL_Criteria _1994_versus_2001.pdf!
! 2! Results and discussion !
In! total! the! IUCN! Red! List! includes! assessments! which!the!impact!of!IAS!was!clearly!indicated!in! for! 9226! species! occurring! in! Europe,! the! narrative! of! the! description! of! the! threats! encompassing! all! taxonomic! groups! (animals,! (but!were!not!coded!accordingly).! plants,! fungi,! bacteria,! chromista! and! protozoa)! According! to! the! IUCN! threats! classification! and! environments! (e.g.! marine,! terrestrial,! freshwater).! Out! of! them,! 1872! species! (20.3%)! scheme,!IAS$represent$the$third$cause$of$threat$ to$ European$ wildlife.! The! first! cause,! affecting! are! considered! as! threatened,! i.e.! classified! as! over! 450! threatened! species,! is! “Dams! &! water! “critically! endangered”! (CR),! “endangered”! (EN)! and!“vulnerable”!(VU).!The!analysis!shows!that!in! management/use”! (coded! 7.2,! under! “Natural' system' modifications”! category)! and! the! second! particular,!354$threatened$species$(229$animals,$ one,! with! over! 400! species! affected,! is! 124$plants$and$1$fungus)$are$specifically$affected$ by$IAS$(which$accounts$for$19%$of$all$threatened$ “Agricultural! &! forestry! effluents”! (coded! 9.3,! under!“Pollution”!category).!This!is!clearly!in!line! species).!The!figures!above!are!the!result!of!the! with! the! evidence! that! the! greatest! threat! to! selection! of! all! species! coded! as! threatened! by! alien! species! (code! 8.1)! in! the! Red! List! biodiversity! is! directly! related! to! the! loss! of! habitat.! The! list! of! the! greatest! threats! to! assessments,! plus! ten! additional! species! for! European!threatened!species!is!shown!in!Fig.!1.!
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7.2!Dams!&!water!management/use! 9.3!Agricultural!&!forestry!effluents! 8.1!Invasive!nonMnalve/alien!species/diseases! 2.3!Livestock!farming!&!ranching! 6.1!Recrealonal!aclviles! 11.2!Droughts! 9.1!Domeslc!&!urban!waste!water! 1.3!Tourism!&!recrealon!areas! 1.1!Housing!&!urban!areas! 7.1!Fire!&!fire!suppression!
0! 50! 100! 150! 200! 250! 300! 350! 400! 450! 500! n°$of$threatened$species$ $
$Figure$1$–$Ranked$list$of$threats$to$the$IUCN$Red$List$assessed$species$in$Europe!
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The!main!groups!of!IAS! responsible!for!the!high! “critically! endangered”! (CR,! 32%),! 112! are! level! of! impact! on! threatened!species!in! Europe! “endangered”! (EN,! 31%)! and! 128! are! are!Vertebrates!(42%;!n=150)!and!Vascular!plants! “vulnerable”!(VU,!36%).!In!figure!2!the!number!of! (Tracheophyta:!34%;!n=120).! species! of! the! main! groups! are! reported! by! category!of!threat.! Considering! the! different! categories! of! threat,! 114! European! species! threatened! by! IAS! are!
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Invertebrates! Vertebrates! Plants!
VU!
EN!
CR!
0! 25! 50! 75! 100! 125! 150! n°!of!species! !
Figure$2$U$Number$of$species$under$each$category$of$threat$sorted$by$higher$taxonomic$group$
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Animal$ species$ account$ for$ 65%$ of$ all$ by! Molluscs! (19%)! and! Arthropods! (5%).! Plants! threatened$taxa$affected$by$IAS.!In!particular,!1! account!only!for!35%!of!the!total!(Figure!3),!most! out! of! 3! threatened! species! of! Freshwater! fish! are!Dicotyledons!(31%).!! appears! affected! by! this! threat! (29%),! followed! !
Fungi! Fish! Plants! 0%! 29%! 35%!
Amphibians! 2%!
Replles! 3%!
Birds! Molluscs! Arthropods! Mammals! 4%! 19%! 5%! 3%!
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Figure$3$–$Percentage$of$species$affected$by$IAS$for$the$main$taxonomic$groups$'
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Among! fish,! those! with! the! highest! number! of! surprising,! given! the! frequent! episodes! of! “critically! endangered”! species! are! Cyprinids! (14! introduction! and! translocation! of! species! from! species),!Salmonids!(10)!and!Acipenserids!(4).!The! other! river! basins! for! angling,! fishery! and! particular! vulnerability! of! fish! to! IAS! is! not! aquaculture.!A!typical!example!is!the!brook!trout!
! 4! (Salvelinus' fontinalis)! a! native! from! North! The! analyses! also! show! that! most! species! America! now! established! in! several! European! threatened!by!IAS!(namely!91%)!are!affected!by! countries,!which!may!compete!for!food!and!cover! one! or! two! alien! species.! Only! 8! species! are! with! and! predate! on! native! fish! such! as! other! affected! by! more! than! 5! alien! species! (namely! salmonids.! Introductions! and! stockings! of! brook! Austropotamobius' pallipes,' Arvicola' sapidus,' trout!have!strongly!affected!the!distribution!and! Pyrrhula'murina,'Salvelinus'fimbriatus,'Salvelinus' structure!of!native!fish!communities,!as!it!might! grayi,' Asparagus' arborescens,' Juniperus' even! replaces! native! salmonids.! In! addition,! the! brevifolia,' Puffinus' mauretanicus).! For! example,! brook!trout!can!hybridise!with!native!brown!trout! the! native! European! whiteMclawed! crayfish! (Salmo'trutta),!and!some!hybrids!are!known!to!be! (Austropotamobius'pallipes),!is!severely!impacted! fertile,! which! can! lead! native! populations! to! a! by! many! introduced! crayfish! among! which! the! loss!of!local!adaptations!and!failure!to!reproduce! red! swamp! crayfish! (Procambarus' clarkii),' and! (Scalera!et'al.!2012).! others! (e.g.' Astacus' leptodactylus,' Pacifastacus' leniusculus,' Orconectes' virilis,' etc).! This! is! the! Very! few! discrepancies! were! highlighted! in! result! of! a! typical! chain! effect! due! to! several! relation! to! the! category! of! threat! at! the! global! concurring!causes.!In!particular,!it!is!thought!that! level.! In! particular,! only! the! following! three! the!North!American!red!swamp!crayfish!(which!is! species! were! assessed! as! more! threatened! in! a!proven!chronic!carrier!of!Aphanomyces'astaci,!a! Europe!than!at!the!global!level:!! fungusMlike!organism!responsible!for!the!soMcalled! • The! False! Ringlet! (Coenonympha' crayfish! plague! in! Europe)! has! led! to! the! oedippus),! a! species! of! butterfly! in! the! accidental! introduction! of! the! crayfish! plague.! Satyridae! family! considered! European! crayfish! species! are! killed! by! this! very! “endangered”! in! Europe,! and! “near! aggressive! pathogen,! so! the! spread! of! this! threatened”!at!global!level.!! disease! in! Europe! has! led! to! the! further! introduction! of! other! replacement! species! of! • The! European! mink! (Mustela' lutreola)! North!American!origin!–!known!to!be!resistant!to! which! is! considered! as! “critically! the!disease!M!for!farming!and!restocking.!The!red! endangered”! in! Europe,! and! swamp! crayfish! is! contributing! to! the! decline! of! “endangered”!at!the!global!level.! the!native!European!crayfish!also!by!replacing!it! • The! Sandarac! Gum! Tree! (Tetraclinis' through! other! mechanisms,! e.g.! competitive! articulata)' which! is! considered! as! exclusion,! differential! susceptibility! to! predation! “endangered”! in! Europe,! and! of! “low! and! reproductive! interference! (Scalera! et' al.! concern”!at!the!global!level.! 2012).! This! is! clearly! a! consequence! of! the! different! The! analyses! of! the! mechanisms! of! impact,! conservation! status! in! different! parts! of! their! range,!which!is!typical!also!in!other!species.!For! identified! for! a! sample! of! 169! animals! and! 202! example,! due! to! its! wide! distribution! in! North! plants,! show! that! competition$ is$ the$ most$ Africa,! the! Sandarac! Gum! Tree! (Tetraclinis' common$ impact$ mechanism$ associated$ to$ IAS$ articulata)! is! assessed! as! “Least! Concern”! threatening$ native$ species$ (40%$ of$ the$ total).$ globally,! although! some! small! subpopulations! This!is!a!very!subtle!type!of!biodiversity!impact,! (Malta! and! Spain)! are! highly! threatened! and! as! it! can! even! affect! the! functioning! of! entire! there!are!some!evidences!of!decline!in!the!main! parts! of! its! range! (Sánchez! Gómez! et' al.! 2015).! ecosystems.! For! example,! the! successful! Otherwise!the!situation!is!quite!the!opposite!for! competition!of!the!alien!zebra!mussel!(Dreissena' the! Thick! shelled! river! mussel! (Unio' crassus),! polymorpha)! against! native! clams! in! the! which' is! more! threatened! at! the! global! level,! freshwater! ecosystem! has! lead! to! local! where! is! considered! as! “endangered”,! than! in! extirpations! of! the! native! molluscs.! In! addition,! Europe,!where!is!considered!as!“vulnerable”.!! its! introduction! to! lakes! in! Europe! and! North!
! 5! America!has!resulted!in!significant!changes!in!the! by! predation! (21%)! and! trampling! (7%).! Other! water! quality! of! the! lakes.! This! invasive! mussel! reported! impact! mechanisms! are! hybridisation! may!thus!have!the!'power'!to!alter!the!structure! (3%),! disease! transmission! (3%! )! and! “Others”,! and!function!of!entire!ecosystems!(Scalera!et'al.! which! include! poisoning/toxicity! (n=4)! and! 2012).! Other! significant! mechanisms! of! impact! parasitism! (n=2).! The! results! are! summarised! in! are! grazing/herbivory/browsing! (24%)! followed! Figure!4.! !
Grazing/! Predalon! herbivory/! 21%! browsing! 24%! Trampling! 7%!
Hybridisalon!! 3%!
Disease! transmission! Compellon! Other! 3%! 40%! 2%! !
Figure$4$U$Impact$mechanisms$of$invasive$species$on$threatened$species.$The$category$“Others”$ includes$parasitism$and$poisoning/toxicity.!
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Some! important! differences! have! been! can! be! characterised! by! devastating! effects.! For! highlighted!by!comparing!mechanisms!of!impact! example,! generalist! predators! such! as! feral! cats! affecting! animals! and! plants! (see! Figure! 5).! For! (Felis' catus),! once! introduced! to! the! wild! (or! example,! competition! is! identified! as! the! main! simply!allowed!to!roam!outdoor),!can!prey!on!a! mechanism! of! impact! for! plants! (i.e.! in! 49%! of! variety!of!native!species,!which!may!suffer!severe! cases! in! this! group)! followed! by! population! declines! and! even! face! extinction.! In! grazing/herbivory/browsing! in! 37%! of! cases.! A! Britain,! for! example,! estimates! derived! from! key! difference! is! that! for! animals! species! scaling!up!local!studies!to!the!national!level!show! competition! is! only! the! second! cause! of! impact,! that!cats!kill!25–29!million!birds!per!year!(Sims!et' accounting! for! 29%! of! cases.! For! this! group! the! al.,!2008).!It!is!easy!to!imagine!how!detrimental! main!cause!of!impact!is!in!fact!predation.!This!is! this! species! can! be,! considering! that! cats! have! not! surprising,! as! predation! is! always! likely! to! been!introduced!practically!everywhere.! pose!a!major!direct!threat!to!native!species,!and!
! 6! 100%! Poisoning/toxicity! 90%! Parasilsm! 80%!
70%! Disease!transmission! 60%! Hybridisalon!! 50%! Trampling! 40%!
30%! Predalon! 20%! Grazing/browsing! 10%! Compellon! 0%! Animals! Plants! !
Figure$5$–$Impact$mechanisms$recorded$for$animals$and$plants.!!
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The! use! of! the! GISD! classification! of! impacts,! context,! as! it! shows! how! the! removal! of! the! allowed!the!assessment!of!the!trends!on!effects! threatening!IAS!can!lead!to!a!prompt!recovery!of! and! outcomes! of! impacts! on! the! basis! of! a! the! population! size! of! the! affected! species! (and! sample! of! 365! records.! The! change! on! species! an! associated! increase! of! the! species! range).! In! distribution! range! (e.g.! in! terms! of! shift,! fact,!this!“threatened”!seabird!has!been!recently! reduction,! etc.)! is! the! most! common! effect! object!of!a!LIFE!project!aimed!at!the!removal!of! (shown! in! 44%! of! cases,! mostly! referred! to! black! rats! (Rattus' rattus)! from! the! island! of! plants).! Invasive! alien! species! like! the! Japanese! Montecristo,!where!the!shearwater!nests!with!an! knotweed! (Fallopia' japonica)! are! a! typical! estimated!population!of!400M750!pairs!(3M10%!of! example! of! species! which! can! have! this! kind! of! the!known!world!population!at!the!time).!In!this! effect,!e.g.!by!transforming!species!diversity!and! case! the! successful! eradication! of! black! rats! physicoMchemical!properties!and!the!structure!of! allowed! 93M95%! of! pairs! to! successfully! fledge! invaded! sites.! For! example,! the! Japanese! juveniles!over!two!years.!As!a!result,!the!number! knotweed! is! known! to! build!up!large!and!dense! of!breeding!pairs!is!expected!to!increase!over!the! monodominant!stands!it!reduces!light!availability! next!ten!years,!with!an!expansion!of!the!breeding! to! the! understorey,! inhibiting! growth! of! woody! colonies!in!the!Tuscan!Archipelago2.!! seedlings! and! shading! out! other! plants,! which! All! the! other! identified! categories! of! effects! results!in!a!delayed!succession.!In!Europe,!dense! stands!that!cover!more!than!1000!m2!are!known.! (outcomes)! are! characterised! by! having! a! direct! impact!on!the!population!of!the!affected!species,! Exclusion! of! accompanying! species! is! also! with!the!only!exception!of!habitat!degradation!or! supported! by! allelochemicals! that! negatively! affect!other!plant!species!(Scalera!et'al.!2012)! complete! replacement/loss! M! with! the! local!
Another! major! effect! of! IAS! on! native! species! is! !!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!! 2! the!decline!in!population!size!(23%!of!cases).!The! http://www.montecristo2010.it/stealthV3_pubblic case! of! the! Yelkouan! shearwater! (Puffinus' a/0840425A0S1345033092.pdf!! yelkouan)! is! particularly! interesting! in! this! ! 7! extinction! of! impacted! species! as! in! the! case! of! carolinensis)!(Bertolino!et'al.!2014)!M!that!reached! the! red! squirrel! (Sciurus' vulgaris)! in! areas! of! 19%!of!cases.!The!overall!data!are!shown!in!the! expansion!of!the!American!grey!squirrel!(Sciurus' Figure!6.!
Populalon!size! decline! Species!range! 23%! change! 44%!
Habitat! Other! degradalon!or! 1%! complete! replacement! Interference! Plant/animal! with! 19%! health! reproduclon! Reduces/! 3%! Changed!gene! inhibits!the! pool/seleclve! 1%! growth!of!other! loss!of! species! genotypes! 6%! 3%! !
Figure$6$U$Impact$outcomes$of$invasive$alien$species$on$threatened$species.$The$“Others”$category$ includes$soil$erosion,$indirect$mortality,$ecosystem$change.$
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The! figure! 7! shows! the! impact! level! of! IAS! on! suffering!from!a!“high”!level!of!impact!due!to!IAS! threatened! species! sorted! by! higher! taxonomic! (e.g.! in! over! 40%! of! the! cases),! followed! by! groups.! Reptiles! are! the! taxonomic! group! molluscs!(over!30%)!and!amphibians.!! characterised! by! the! highest! number! of! species!
! 8! 100%! Unknown! 90%! low! 80%! medium! 70%! high! 60%! 50%! 40%! 30%! 20%! 10%! 0%!
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Figure$7$U$Impact$level$on$threatened$species$on$a$selection$of$higher$taxonomic$groups.$!
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But! which! are! the! main! alien! species! posing! a! family!Rodentia)!are!considered!as!a!threat!to!a! threat! to! European! biodiversity?! A! complete! list! total! of! 27! native! species! (among! which! birds,! of! invasive! alien! species! is! reported! in! Annex! 1.! mammals,!reptiles,!molluscs!and!plants).!! Since! in! a! number! of! situations! it! was! not! ! possible! to! identify! the! responsible! species! In! figure! 8! the! invasive! species! that! have! an! precisely,! the! data! reported! are! related! to! the! impact!on!threatened!species,!separated!on!the! best! available! information! (e.g.! genus! or! higher! basis! of! by! the! main! taxonomic! groups,! are! taxonomic! group).! Information! on! number! of! shown:! regarding! animals,! fish! are! the! largest! (native)!European!threatened!species!affected!by! group! with! 26! species! and! 3! different! genus! each! invasive! alien! species! is! also! reported.! For! identified! as! a! threat! (24%),! followed! by! example,! rodents! (indicated! in! the! dataset! as! mammals! (23%). Rattus'rattus,!Rattus'norvegicus,'Rattus!spp.!and! !
!
! 9! Fish! 24%! Mammals! 23%!
Plants! Arthropods! 31%! 8%!
Other! Herps! Molluscs! 5%! 5%! 4%! !
Figure$8$–$Alien$species$that$affect$threatened$species$sorted$by$group.$“Others”$category$includes$ birds,$viruses,$fungi$and$jellyfish.!
!
Invasive! alien! mammals! M! despite! the! relatively! which!are!“critically!endangered”.!In!table!1!the! small! number! of! species! identified! as! a! threat! details!on!the!total!number!of!threatened!species! (n=23)!M!are!the!group!associated!with!the!highest! affected! by! each! alien! group! are! shown! (data! number! of! threatened! species! in! Europe! (141,! sorted!by!category!of!threat!are!also!provided).! corresponding! to! 40%! of! total),! one! third! of! !
Table$1$–$Number$of$threatened$species$impacted$by$each$group$of$IAS! Alien$species$$ VU$ EN$ CR$ Total$no.$of$impacted$native$ species! Mammals! 46! 46! 49! 141! Fish! 48! 27! 35! 110! Plants! 35! 39! 34! 108! Arthropods! 4! 8! 3! 15! Molluscs! 3! 5! 5! 13! Reptiles!and!amphibians! 3! 2! 1! 6! Others! 3! 5! 1! 10! !
In!total,!96!different!IAS!have!been!identified,!56! In! total,! four! feral! domestic! species! (the! goat! of!which!are!aliens!to!Europe!while!40!are!aliens! Capra' hircus,' wild! pig' Sus' scrofa,' domestic! cat! only!in!part!of!Europe.!Invasive!alien!species!are! Felis' catus' and! domestic! dog' Canis' familiaris)! in!some!cases!indicated!in!the!source!dataset!at! have!been!included!in!the!list,!but!only!when!the! either!the!genus!level!or!the!family!level.!In!fact,! code! assigned! in! the! IUCN! Red! List! did! clearly! besides!the!96!species,!there!are!additional!data! refer!to!the!IAS!threat!(e.g.!sometime!the!goat!is! relative! to! 4! families! and! 15! genus! of! IAS! classified! under! code! 2.3! “grazing”! like! sheep,! representing!a!threat.!! livestock!etc.!in!which!case!was!not!considered).! Actually,! also! the! rabbit! should! be! considered!
! 10! feral,! as! most! of! the! introductions! were! carried! devastating)! coloniser! around! the! world,! it! is! out! since! ancient! times! with! animals! from! threatened!within!its!native!range!(Lees!and!Bell,! domestic!origin3.! 2008).!!
Considering! only! the! alien! species! identified,! 17! The! introductions! of! mammals,! such! as! goats,! and! 16! are! present! in! the! IUCN! list! of! “One! rabbits,!and!cats,!are!typical!case!studies!used!to! Hundred! of! the! World's! Worst! Invasive! Alien! highlight!the!consequences!of!the!impact!of!alien! Species”!and!in!the!DAISIE!“One!Hundred!of!the! mammals,!particularly!in!island!ecosystems.!Such! Europe's! Worst! Invasive! Alien! Species”! introductions! are! known! to! have! caused! the! respectively!(to!be!noticed!that!in!the!European! severe!regression!of!native!and!endemic!species,! list,!feral!species!are!not!considered).! of!both!fauna!and!flora.!In!some!cases!goats!and! rabbits! also! led! to! heavy! erosion,! e.g.! along! the! In!Table!2!invasive!alien!species!that!affect!more! coastlines,! which! in! turn! caused! problems! for! than! 4! threatened! species! are! reported! (species! nesting! sites! of! several! marine! birds.! It! is! not! precisely! identified,! or! generic! categories! remarkable!that!to!address!this!problem,!specific! such! as! animals! and/or! plants! or! groups! projects! have! been! implemented! particularly! identified!only!at!family!and!genus!level!were!not! through! the! LIFE! programme,! e.g.! in! Deserta! considered! in! this! analysis).! The! most! impacting! Grande! (in! the! Madeira! archipelago,! Portugal)! species!is!the!feral!goat!(Capra'hircus),!followed! both! rabbits! and! goats! were! successfully! by! the! rabbit! (Oryctolagus' cuniculus)! and! the! 4 eradicated,!along!with!cats .!It!was!the!first!time! feral!cat!(Felis'catus).!These!are!all!domesticated! in! Europe! that! such! an! eradication! programme! species,!particularly!damaging!in!insular!contexts.! targeting!invasive!alien!animals!was!attempted!in! All! those! very! impacting! species! are! alien! to! an!island!at!this!scale.!! Europe,! with! the! only! notable! exception! of! the! rabbit.! In! fact! the! rabbit! is! native! to! southern! It!is!likely!that!as!the!information!on!the!impact! Europe! (Iberian! Peninsula)! and! possibly! of!IAS!will!be!systematically!collected!in!the! Northwest! Africa.! For! this! reason! this! species! is! future,!e.g.!also!in!relation!to!the!implementation! also! considered! a! 'conservation! paradox',! for! of!the!new!EU!Regulation!on!IAS,!the!analysis!will! although! it! is! a! highly! successful! (usually! provide!a!more!precise!assessment!of!this!threat.! !!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!! For!example,!it!is!not!clear!whether!the!impact!of! 3 ! Some!confusion!may!be!linked!to!the! the!Chytrid!fungus!on!amphibians!is!actually! nomenclature!used!for!the!mouflon,!because!many! underestimated.!In!the!database!used!for!this! names!are!(sometime!wrongly)!used!as!synonyms!in! study!only!two!species!seem!affected!by!this! the!existing!literature,!e.g.!Ovis'ammon,'O.'aries,'O.' threat,!namely!the!Apennine!yellowMbellied!toad! orientalis.!For!the!mouflon,!semiMdomestic!sheep! (Bombina'pachypus)!and!the!Sardinian!brook! introduced!in!ancient!time!in!CorsicaMSardinia,!and! then!translocated!for!hunting!purposes!in!many!other! salamander!(Euproctus'platycephalus).!However,! areas!–!the!most!correct!scientific!name!is!Ovis'aries.! this!is!not!consistent!with!the!current!estimates! In!fact!Ovis'orientalis!is!a!subspecies!of!Ovis'aries.! that!about!92!%!of!amphibians!considered! However,!Ovis'aries!is!also!used!for!indicating!the! “critically!endangered”!by!the!IUCN!Red!List!are! domestic!sheep!(from!which!the!mouflon!actually! undergoing!declines!that!might!be!linked!to! originated).!Some!experts!may!have!different! Batrachochytrium'dendrobatidis'(Bd).!In!fact,!also! interpretations,!in!fact!the!mouflon!is!sometime! referred!to!also!as!Ovis'ammon,!but!this!species! !!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!! should!refer!only!to!the!argali,!which!has!never!been! 4! !Restoration!measures!for!the!terrestrial! introduced!outside!its!natural!range!(definitely!not!in! habitat!of!Deserta!Grande!(LIFE95!NAT/P/000125)! Europe).!This!might!create!further!confusion! http://ec.europa.eu/environment/life/project/Project http://www.vertebrates.si.edu/msw/mswcfapp/msw/ s/index.cfm?fuseaction=search.dspPage&n_proj_id=3 taxon_browser.cfm?msw_id=13213! 8&docType=pdf!
! 11! in!Europe!we!know!that!over!one!third!of! monitor!and!possibly!prevent!the!further! amphibian!species!have!the!pathogen!present,! introduction!of!IAS.!Additionally,!the!recent! and!at!least!10!%!of!the!native!ones!are!involved! emergence!of!another!chytrid!fungus,!B.' in!chytridiomycosisMdriven!decline,!not!only!in! salamandrivorans,!which!also!causes! yellowMbellied!toads!and!Sardinian!brook!newts! chytridiomycosis!and!death!in!salamanders! (Scalera!et'al.!2012).!The!Bd,!which!is!included!in! (Martel!et'al.,!2013),!shows!how!dynamic!the! the!list!of!“One!Hundred!of!the!World's!Worst! overall!situation!is,!and!stresses!the!importance! Invasive!Alien!Species”,!is!actually!spread!by! to!ensure!that!a!picture!on!the!state!of!the!art!of! other!IAS,!such!the!American!bullfrog!(Lithobates' IAS!impact!on!native!species!in!Europe!is!taken! catesbeianus)!and!other!amphibians!traded!as! regularly!across!the!years.! pets!in!Europe,!showing!the!importance!to! !
Table$2$–$Invasive$alien$species$impacting$more$than$4$threatened$species.$$
100!of$the! Tot$n°$of$ 100$of$the$ worst$$ Alien!species$ CR$ EN$ VU$ impacted$native$ worst$GISD$ DAISIE! species! yes! ! Capra'hircus! 11! 7! 9! 27! yes! ! Oryctolagus'cuniculus! 14! 7! 5! 26! yes! ! Felis'catus! 5! 5! 3! 13! ! yes' Neovison'vison! 1! 2! 4! 7! ! ! Ovis'aries! 1! 5! 1! 7! ! ! Ammotragus'lervia! 1! 3! 2! 6! ! yes' Opuntia'ficusLindica! 1! 3! 2! 5! ! ! Pennisetum'setaceum! 4! 1! 0! 5! ! yes' Procambarus'clarkii! 0! 3! 2! 5! !
! 12! Conclusions !
This! review! provides! an! updated! and! sp5)!causes!impacts!on!at!least!13!native!species,! comprehensive!analysis!on!the!impact!of!invasive! seriously! endangering! the! coastal! dune! species!on!European!native!species.!The!study!is! ecosystems!in!Southern!Europe.!Indeed!ice!plants! based! on! an! inMdepth! analysis! of! two! key! IUCN! are!known!to!have!a!major!impact!on!ecosystem! knowledge!products,!namely!the!IUCN!Red!list!of! services! as! a! consequence! of! the! growth! of! Threatened! Species,! and! the! Global! Invasive! dense,! impenetrable! and! monodominant! mats! Species!Database!(GISD).!! which! may! cover! large! areas,! reducing! local! biodiversity!by!direct!competition!with!native!and! According! to! the! best! data! available! at! the! often!endangered!coastal!plant!species.! European! level,! invasive$ alien$ species$ (IAS)$ are$ the$ 3rd$ most$ severe$ threat$ to$ European$ The! American! mink! (Neovison' vison)' is! another! threatened$ species,! after! dams! and! water! species!of!great!concern!as!it!directly!impacts!at! management,!and!agricultural!forestry!effluents.! least! 7! endangered! native! species.! In! particular! The! results! of! the! review! show! that! 1$ out$ of$ 5$ this! predator! is! the! greatest! threat! to! the! rare! threatened$species$in$Europe$is$directly$affected$ and! “critically! endangered”! European! mink! by$ invasive$ alien$ species.! In! particular! 145! (Mustela'lutreola),!one!of!the!only!two!endemic! “critically! endangered”! species,! 112! carnivore! species! of! Europe,! and! other! small! “endangered”! species! and! 128! “vulnerable”! vertebrates,!including!birds!and!amphibians.!! species! are! affected! by! IAS.! Animals! are! usually! more! impacted! than! plants,! with! fish$ being$ The! outcomes! of! the! present! assessment,! focused!on!“threatened”!species!sensu'IUCN!Red! particularly$affected$by$this$threat:!35!“critically! List,! partly! differ! from! the! results! of! the! recent! endangered”!species!belonging!to!this!taxonomic! group,! along! with! 27! “endangered”! and! 48! “State!of!nature!in!the!EU”!(EC!2015,!EEA!2015),! focused!on!species!and!habitats!protected!under! “vulnerable”!species,!are!impacted!by!IAS.!! the! Birds! and! Habitats! Directives,! describing! IAS! The!main$mechanism$of$impact$by$invasive$alien$ as! a! less! significant! threat! compared! to! other! species$is$competition!(accounting!for!40%!of!all! causes! of! harm.! The! different! outcomes! are! in! cases),!followed!by!grazing,!and!predation.!Feral$ part!due!to!the!different!geographic!scope!which! domestic$ species$ introduced$ by$ humans$ are$ a$ characterises!the!two!approaches,!but!mostly!to! serious$ threat$ in! several! European! contexts;! for! the!different!set!of!species!(and!habitats)!which! example,!feral!goats!are!a!concrete!threat!to!11! the! analysis! refer! to.! In! fact,! only! 43.5%! of! “critically! endangered”! species,! 7! “endangered”! species! protected! under! the! Habitats! and! Birds! species! and! 9! “vulnerable”! species.! This! is! not! Directives!are!assessed!as!threatened!under! the! surprising,! as! goats! are! well! known! to! be! voracious! herbivorous! which! may! destroy! the! !!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!! 5!There!is!some!controversy!about!the!taxonomic! vegetation! of! entire! territories,! turning! dense! identity!of!invasive!alien!ice!plants.!Although!most! vegetated!areas!into!a!desolated!desert.! records!are!attributed!to!Carpobrotus'edulis,! another!introduced!ice!plant!species!(namely!C.' Some! nonMferal! invasive! species! are! also! acinaciformis)!occurring!in!Europe,!is!actually!more! particularly! harmful,! impacting! high! number! of! widespread!than!C.'edulis.!Additionally'!both! native! species.! Rats! are! a! major! threat! to! many! 'species'!hybridise!and!form!a!hybrid!complex!with! critically! endangered! seabirds! and! reptiles! (the! intermediate!characters!(see!Scalera!et'al.!2012).! genus! endemic! of! the! Canary! islands,! Gallotia! Therefore!the!analyses!were!carried!out!at!the! sp.).! Among! plants,! the! ice! plant! (Carpobrotus' genus!level.!
! 13! IUCN! Red! List! (in! particular! 465! threatened! greater!concern!for!“threatened”!species,!rather! species!on!a!total!of!1069!species!included!in!the! than! “protected”! species! such! as! those! covered! Nature! Directives).! This! shows! that! IAS! are! of! by!the!EU!Nature!Directives.!! !
!
! 14! References !
Bertolino!S.,!di!Montezemolo!N.C.,!Preatoni!D.G.,! Europe.!Invading!Nature:!Springer!Series!in! Wauters! L.A.,! &! Martinoli! A.! (2014)! A! grey! Invasion! Ecology,! Springer,! Dordrecht,! The! future! for! Europe:! Sciurus! carolinensis! is! Netherlands,!Pp.!119M129! replacing! native! red! squirrels! in! Italy.! Biological!Invasions,!16,!53–62.!! Genovesi!P.!&!Shine!C.!(2004)!European!Strategy! on! Invasive! Alien! Species.! Nature' and' Butchart!S.H.M.,!Walpole!M.,!Collen!B.,!van!Strien! environment,!161,!1–73.!! A.,! Scharlemann! J.P.W.,! Almond! R.E.A.,! Baillie!J.E.M.,!Bomhard!B.,!Brown!C.,!Bruno! Kettunen!M.,!Genovesi!P.,!Gollasch!S.,!Pagad!S.,!&! J.,! Carpenter! K.E.,! Carr! G.M.,! Chanson! J.,! Starfinger!U.!(2009)!Technical!support!to!eu! Chenery! A.M.,! Csirke! J.,! Davidson! N.C.,! strategy! on! invasive! alien! species! (IAS)! Dentener! F.,! Foster! M.,! Galli! A.,! Galloway! Assessment!of!the!impacts!of!IAS!in!Europe! J.N.,!Genovesi!P.,!Gregory!R.D.,!Hockings!M.,! and!the!EU.!! Kapos!V.,!Lamarque!J.MF.,!Leverington!F.,!Loh! J.,! McGeoch! M.A.,! McRae! L.,! Minasyan! A.,! Lees,! A.C.! and! Bell,! D.J.,! 2008,! 'A! conservation! Morcillo! M.H.,! Oldfield! T.E.E.,! Pauly! D.,! paradox!for!the!21st!century:!the!European! Quader!S.,!Revenga!C.,!Sauer!J.R.,!Skolnik!B.,! wild! rabbit! Oryctolagus' cuniculus' ,! an! Spear! D.,! StanwellMSmith! D.,! Stuart! S.N.,! invasive! alien! and! an! endangered! native',! Symes!A.,!Tierney!M.,!Tyrrell!T.D.,!Vié!J.MC.,! Mammal!Review!,!(38)!304–320.! &! Watson! R.! (2010)! Global! Biodiversity:! Maran,!T.,!Skumatov,!D.,!Palazón,!S.,!Gomez,!A.,! Indicators!of!Recent!Declines.!Science'(New' Põdra,!M.,!Saveljev,!A.,!Kranz,!A.,!Libois,!R.! York,'N.Y.),!328,!1164–1168.!! &!Aulagnier,!S.!(2011)!Mustela'lutreola.!The! IUCN! Red! List! of! Threatened! Species.! Clavero! M.! &! GarcíaMBerthou! E.! (2005)! Invasive! Version! 2014.3.!
! 15!
Scalera! R,! Genovesi! P,! Essl! F,! Rabitsch! W,! 2012.! The! impacts! of! invasive! alien! species! in! Europe.!EEA!Technical!report!no.16/2012.!!
Sims,! V.,! Evans,! K.L.,! Newson,! S.E.,! Tratalos,! J.A.! and! Gaston,! K.J.,! 2008,! Avian! assemblage! structure! and! domestic! cat! densities! in! urban! environments.! Diversity! &! Distributions!,!(14)!387–399.!
Vilà! M.,! Basnou! C.,! Pysek! P.,! Josefsson! M.,! Genovesi!P.,!Gollasch!S.,!Nentwig!W.,!Olenin! S.,!Roques!A.,!Roy!D.,!Hulme!P.E.,!&!DAISIE! partners!(2010)!How!well!do!we!understand! the! impacts! of! alien! species! on! ecosystem! services?! A! panMEuropean,! crossMtaxa! assessment.! Frontiers' in' Ecology' and' the' Environment,!8,!135–144.!!
! 16! Annex 1 - Complete list of alien invasive species and groups that affect threatened (IUCN Red List CR, EN, VU) species in Europe ! No.$of$ Rattus'norvegicus' 2! Alien$species$or$group$ impacted$ Salvelinus'alpinus' 2! native$species$ Scardinius'erythrophthalmus' 2! Unspecified!species! 83! Silurus'glanis' 2! Unspecified!Fish! 51! Squalius'cephalus' 2! Unspecified!Plants! 36! Tinca'tinca' 2! Unspecified!Animals! 28! Unspecified!molluscs! 2! Capra'hircus' 27! Vulpes'vulpes' 2! Oryctolagus'cuniculus' 26! Acacia'dealbata' 1! Carpobrotus'spp.' 13! Acacia'saligna' 1! Felis'catus' 13! Acipenser'stellatus' 1! Rattus'spp.! 12! Ageratina'adenophora' 1! Family!Rodentia! 10! Anguillicoloides'crassus' 1! Neovison'vison' 7! Aphanomyces'astaci' 1! Ovis'aries' 7! Arundo'donax' 1! Ammotragus'lervia' 6! Astacus'leptodactylus' 1! Family!Salmonidae! 6! Azolla'filiculoides' 1! Pennisetum'setaceum' 6! Bison'bison' 1! Coregonus'spp.! 5! Cannabis'sativa' 1! Opuntia'ficusLindica' 5! Chaetorellia'spp.! 1! Opuntia'spp.! 5! Chondrostoma'genei' 1! Procambarus'clarkii' 5! Chrysemys'picta' 1! Agave'spp.! 4! Cobitis'arachthosensis' 1! Esox'lucius' 4! Cottus'gobio' 1! Potamopyrgus'antipodarum' 4! Cuscuta'spp.! 1! Rutilus'rutilus' 4! Eucalyptus'globulus' 1! Abramis'brama' 3! Eucalyptus'spp.! 1! Agave'americana' 3! Family!Mustelidae! 1! Family!Leporidae! 3! Fundulus'heteroclitus' 1! Gambusia'spp.' 3! Genetta'genetta' 1! Hedychium'gardnerianum' 3! Gymnocephalus'acerina' 1! Ondatra'zibethicus' 3! Herpestes'javanicus' 1! Pittosporum'undulatum' 3! Huso'huso' 1! Rattus'rattus' 3! Icerya'purchasi' 1! Sander'lucioperca' 3! Impatiens'spp.! 1! Sus'scrofa' 3! Lantana'camara' 1! Theba'pisana' 3! Larus'cachinnans' 1! Ailanthus'altissima' 2! Leuciscus'cephalus' 1! Canis'familiaris' 2! Lithobates'catesbeianus' 1! Capra'aegagrus'cretica' 2! Martes'spp.! 1! Centranthus'ruber' 2! Melanoides'tuberculata' 1! Chondrostoma'nasus' 2! Mesembryathemum'crystallinum' 1! Chytrid'Batrachochytrium'dendrobatidis' 2! Micropterus'spp.! 1! Clethra'arborea' 2! Mnemiopsis'spp.! 1! Corbicula'fluminea' 2! Mus'musculus' 1! Cotesia'Glomerata' 2! Mus'spp.! 1! Cryptomeria'japonica' 2! Natrix'maura' 1! Gymnocephalus'cernuus' 2! Orconectes'limosus' 1! Micropterus'salmoides' 2! Orconectes'virilis' 1! Myocastor'coypus' 2! Oxyura'jamaicensis' 1! Ovis'aries'(domestic!sheep)! 2! Pararge'aegeria' 1! Pacifastacus'leniusculus' 2! Pelargonium'spp.! 1! Perca'fluviatilis' 2! Pennisetum'spp.! 1! ! 17! Phalaris'aquatica' 1! Sagittaria'subulata' 1! Pinus'halepensis' 1! Salmo'letnica' 1! Pinus'radiata' 1! Senecio'angulatus' 1! Podarcis'siculus' 1! Smilax'aspera' 1! Poxvirus'avium' 1! Thelohania'contejeani' 1! Procyon'lotor' 1! Theodoxus'fluviatilis' 1! Pseudochondrostoma'polylepis' 1! Trachemys'scripta' 1! Ranunculus'spp.! 1! Unspecified!Anura! 1! Rhododendron'spp.! 1! Unspecified!Crustaceans! 1! Rubus'spp.! 1! Unspecified!Mammals! 1! Rutilus'rubilio' 1!
! 18!