TrophicTrophic relationsrelations inin thethe LowerLower RhineRhine foodfood webweb duringduring invasioninvasion andand afterafter establishmentestablishment ofof DikerogammarusDikerogammarus villosusvillosus

M.C. van Riel, G. van der Velde and A. bij de Vaate

Dept.Dept. ofof Animal EcologyEcology and and Ecophysiology, Ecophysiology, UniversityUniversity of of NijmegenNijmegen RIZARIZA SuccessfulSuccessful invasionsinvasions ofof thethe RhineRhine duedue tototo:::

-increased-increased connectivityconnectivity ofof largelarge EuropeanEuropean riversrivers -antropogenic-antropogenic stressstress asas pollution,pollution, intensifiedintensified shippingshipping -reduction-reduction ofof ecotypeecotype heterogeneityheterogeneity byby highhigh modificationmodification ofof thethe streamstream bedbed

ResultResultResult:::

-high-high turnoverturnover ofof amphipodamphipod invasionsinvasions

WhatWhat isis thethe effecteffect onon thethe RhineRhine foodfood web?web? AmphipodAmphipod dominancedominance inin thethe RhineRhine

GammarusGammarus tigrinustigrinus 19821982

ChelicorophiumChelicorophium curvispinumcurvispinum 19871987

EchinogammarusEchinogammarus ischnusischnus 19891989

DikerogammarusDikerogammarus villosus villosus 19951995 DikerogammarusDikerogammarus villosusvillosus

…cette bête a une énorme mâchoire qui lui permet de tout gober sur son passage… www.cybersciences.com/

…The shrimp, villosus, characterized as "mini-Jaws", attack small fish and feast on native species, some with shells, by biting and shredding their victims… www.glu.org

…Scientists say they fear an invasion of killer shrimp could spell the end for some native species in the . The predator -- known to scientists as dikerogammarus villosus or pink peril -- has chewed its way across various parts of Europe in recent years… http://www.threegorgesprobe.org

…Dikerogammarus villosus - the killer shrimp that hunts fish … asp.wlv.ac.uk

This Ponto-Caspian gammarid is clearly presumed to have a huge influence on the ecosystem it invades We compared the food web during invasion in ’96-’98 (Marguillier et al., 1998) with the Rhine food web after establishment of D. villosus (’01-’03) using

StableStable isotopeisotope analysisanalysis

-stable isotopes (δ13C, δ15N) of food items are assimilated in consumers muscle tissue -based on the actual food assimilation of a species -provides information on the longterm diet -δ13C indicates original source (enrichment 1 ‰ on average) -δ15N indicates trophic position (enrichment 3 ‰ on average) Rhine food web ’96-’98 (Marguillier et al., 1998)

plant and organic matter 20 macroinvertebrates fish

18 Fish

16 Es Dv macroinvertebrates Cfa C ) ) Cfs 14 Ccu ‰ ‰ Dp Cc 15N ( 15N ( δ δ T 12 S

Phyt POM 10

8 Phytoplankton, POM, moss and Plumatella and silt lamprey

6 -34 -32 -30 -28 -26 -24 -22 -20 -18 -16 -14 δ13C ( ‰) Rhine food web ’01-’03 (after establishment)

macroinvertebrates 20 parasitic species plants and organic matter 18 Top predators (eg fish) fish Jaera istri D. villosus life stages 16 Lfad

Es 14 Ji Ol macroinvertebrates Ponto-Caspian 12 ) ) Ji ‰ ‰ Dv Ei Ccu 10 Cfa Dp Gt 15N ( 15N ( T δ δ Cfs C Lfj Pm Algae1 8

mud 6

Pm 4 Organic matter and aquatic plant matter

2 det Riparian plants

0 -34 -32 -30 -28 -26 -24 -22 -20 -18 -16 -14 δ13C ( ‰) δ 13 C δ 15 N

1996-1998 1996-1998 8 Fish 8 macroinvertebrates 7 7 aquatic plant 6 terrestic plant 6 organic 5 5

4 4

3 3 Frequency (#) Frequency Frequency (#) Frequency 2 2

1 1

0 0 -10 -16 -17 -18 -19 -20 -21 -22 -23 -24 -25 -26 -27 -28 -29 -30 -31 -32 -33 -34 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 δ13C ( ‰) δ15 N ( ‰)

2001-2003 2001-2003 8 8

7 7

6 6

5 5

4 4

3 3 Frequency (#) Frequency Frequency (#) Frequency 2 2 1 1 0 0 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 -16 -17 -18 -19 -20 -21 -22 -23 -24 -25 -26 -27 -28 -29 -30 -31 -32 -33 -34 δ15N ( ‰) δ13C ( ‰) Macroinvertebrate food web after correction for ∆ 15 N based on values of Cfa, Cfs and Dp (according to Cabana et al., 1996; Vander Zanden et al., 1999)

21

20 Pl 19 Es

18 Ol Af ) ) 17 ‰ ‰ Es Pl 16 Ad 15N ( 15N ( Hb Po Dvbig δ δ Ol H Ccu Dv Dvad 15 Dv Dvj Cfs Cfa C Gt Cfa Ef Bt 14 C Cfs Dp Dp Ccu Hp Cc Bryo 13 Gt Pr

12

11 -32 -31 -30 -29 -28 -27 -26 -25 δ13C ( ‰) Theoretical prey range based on δ13C - δ15N content

17

16 Pl Pl Dvbig Ad Hb Po Ccu Ol H Ccu Dvad 15 Dv Dvj Dv Gt

) C

) C Cfs Cfa ‰ ‰ Cfa Dp Ef Bt C Cfs 14 Ccu 15N ( 15N ( Dp δ δ Hp Cc Bryo

Gt 13 Pr

12

11 -32 -31 -30 -29 -28 -27 -26 -25 δ13C ( ‰) :Omnivores: DietDiet dependsdepends onon preferencepreference andand food food availabilityavailability …………andand maymay affectaffect preyprey communitiescommunities EcotypesEcotypes RhineRhine

I

High invaders impact

II

Poorly inhabited Macroinvertebrates on the stones

Species found: 80000 70000

other species 60000 Ancylus fluviatilis 50000 40000 Dreissena polymorpha 30000 Jaera istri (#m-2) density 20000 Gammarus tigrinus 10000 Echinogammarus ischnus 0 June 1998 July 1998 August 1998 September Dikerogammarus villosus 1998 80000 Chelicorophium curvispinum 70000

60000

50000

40000

30000 density (#m-2) density 20000

10000

0 June 2001 July 2001 August 2001 September 2001 Acaridae

Nemertinea Oligochaeta stones stones ** ** Hypania invalida the the * * Dendrocoelum romanodanubiale

Insecta other Bivalvia ** ** other Gastropoda * * Ancylus fluviatilis ** ** Dreissena polymorpha Jaera istri Gammarus tigrinus * * Echinogammarus ischnus Dikerogammarus villosus ** ** Macroinvertebrates on Macroinvertebrates on Chelicorophium curvispinum ** Chelicorophium curvispinum ** 0 0 1500 3000 4500 3000 1500 1500 3000 4500 3000 1500 - - - - 90000 91000 92000 93000 94000 95000 90000 91000 92000 93000 94000 95000 ------

Changes in density (# m -2 ) ConclusionsConclusions

--the the RhineRhine foodfood webweb isis highlyhighly influencedinfluenced byby invadersinvaders

--the the RhineRhine foodfood webweb isis fuelledfuelled bybyPOM, POM, phytoplanktonphytoplankton andand riparianriparian vegetationvegetation

--omnivores omnivores,, filterfilter --,, depositdeposit-- and and detritusdetritus-feeders-feeders functionfunction asas keystonekeystone speciesspecies inin transferringtransferring energyenergy toto higherhigher trophictrophic levelslevels

--invader invader speciesspecies functionfunction asas ecosystemecosystem engineersengineers,, determiningdetermining functionalfunctional diversitydiversity,, communitycommunity-- and and foodfood webweb structurestructure ThanksThanks toto

JelleJelle Eygensteijn,Eygensteijn, SandraSandra Marguillier,Marguillier, SanjeeviSanjeevi Rajagopal,Rajagopal, MarijMarij Orbons,Orbons, MartinMartin Versteeg,Versteeg, FreekFreek Kluitmans,Kluitmans, Barry Barry Kelleher,Kelleher, thethe staffstaff ofof researchresearch vesselsvessels ‘the ‘the Conrad’Conrad’ andand ‘the‘the Schollevaer’Schollevaer’ RIVORIVO && RIZARIZA

Species found: Macroinvertebrates on the sand

other species 1000 900 Oligochaeta 800 Chironomidae 700 600 Lampetra fluviatilis 500 400

Corbicula fluminalis (#m-2) density 300 Corbicula fluminea 200 100 Gammarus tigrinus 0 Echinogammarus ischnus June 1998 July 1998 August 1998 September 1998 Dikerogammarus villosus 1000 Chelicorophium curvispinum 900 800 700 600 500 400

density (#m-2) density 300 200 100 0 June 2001 July 2001 August 2001 September 2001 * * Lampetra fluviatilis Ephemeroptera Odonata Heteroptera Trichoptera sand sand Nematoda Hirudinea the the Tricladida Annelida * * Oligochaeta Hypania invalida ** ** Chironomidae Sphaeriidae * * Gastropoda Corbicula fluminalis Corbicula fluminea * * Dreissena polymorpha * * Jaera istri Gammarus tigrinus Macroinvertebrates on Macroinvertebrates on Echinogammarus ischnus * * Dikerogammarus villosus * * Chelicorophium curvispinum 0 0 500 400 300 200 100 100 500 400 300 200 100 100 - -

Changes in density (#m -2 ) Rhine food web ’96-’98 (Marguillier et al., 1998)

plant and organic matter 20 macroinvertebrates fish

18 Sl Cg Pfl Gc Gg Fish Pf AaBb Aas Oe Se 16 Dv Es Rr Ct Ad Ga Aal Pl Lc macroinvertebrates Hs Ab Ol Cfa C Ef Cfs Cn Bt Cca 14 Ccu Dp Cc Cp Pr 15N ( ‰) δ T 12 S Lfad Cg Phyt POM 10

Lfj Pf

8 Plumatella, silt and POM, moss and phytoplankton lamprey

6 -34 -32 -30 -28 -26 -24 -22 -20 -18 -16 -14 δ13C ( ‰) Rhine food web ’01-’03

macroinvertebrates 20 pa ra si tic spe cie s plants and organic matter Top predators (eg fish) fish 18 Jaera istri D. villosus life stages Lfad 16 Sl Ab Pl Bb Es Jiw 14 Pf Rr Ol macroinvertebrates macroinvertebrates Pogem Ponto-Caspian species Af Ps 12 DVbig Po DVad Hb Jis DVj Dv Hd moss Cfa Ccu 10 Dp Gt 15N ( ‰) ( 15N Lfj Ei T δ C Cfs Aa Pm Algae1 Hp Bryo 8 Cn

6 Pp mud Cg Cs Fg Pm Ea Ls 4 Rf Sp Organic matter and aquatic plant matter Ec Rs Ca 2.80To 2 det Ripparian plants Am Ce Ripparian plants

0 -34 -32 -30 -28 -26 -24 -22 -20 -18 -16 -14 δ13C ( ‰)