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Institute of Science, Rehovot 76100, lsrael tFluid Dynamics Laboratory, Unive15ity ol H!ll, East Yorkshire HU67RX, UK
I
2 3. Fa|aday, M. Chladni, E l.

5.

P hi l. lh ns. R. soc. |on d. 121, 299 - 31 8 <1a31). Thona5, 8. & sq'iifs A. M phys Rev Lefl a1,574-571 <1998). Ray eish,t.Phil fnnt. R. Soc. ttnd. A 175,1(1883) KinE,L.V. he R. sat Land. 4147, 212-216, 11935).

t azday, M.

ir moribund or dead L. delineatus was 67/o (n=17). Tbe parasite war also detected in subclinical ffsh in the treatment
like agent
group, but at a lower prevalen.e (28o/o; tt=32). This level ofinfection is consistent with that reported in tissus of salmon erposed to S. desttuenl.

phil Tanr
F.

R.

Soc.

Lond.121,119-140 (1831).
Theotie des Klo ng?n

Enttl.ckunsen
A

ub.t die
study
in

(Wltlenberg,l787) Watler M. Chtodni tiguft\: London,l96l)

Synnetty

(8e11,

accornpaniei Ihi! co'nmur cil onon Nan/er!r.ib. te Comp.tf ngtf nrn.lal Ints..t.t lccl at ed n(rt1e.

Suppl.n

nlary

inlo!6.ll.n

dot1A1038/4ir1145d

Preliminary examinatior indicates that

other clprinids, such as the fathead minnow Pimephales promelas, are also susceptible to this pathogen, which causes effecis identicalto those i.n L, delineatus (prevalence,20ok, n=5). All P parw specimens (r=10) tested for the
rosette-like agent lvere negative however, thia is to b expected, giver that pathogen concentrations in healthy carrier fish are very lora and difffcult to detect using conventional diagnostic tests'. Cohabitatior 6 tudies ate a tecognized tnethod for detecting cfrier states fot differ^ ent fish pathogense'0 and, as our results illustrate, they are currentlythe most reliable way to detect a healthy carrier, Our resllts have three impo ant irnpllcations. First, the most inva$ive fish specie$ rn Europe{ is a healthy host for a deadly, nonspeciffc pathogen that could threaten aquaculture tradg including that ofsalmonids. Secotrd,
are carriers ofpathogens.

BIODIVERSITY

Disease threat to European fish

The deliberate introduction of nen'species can have unexpected negative consequencesll and we showhere how a recently introduced fish, the invasive Asian cvorinid Pseudorasbon porva, h lsing increased mortality and

totally inhibitirg spawning in an already

endangered native fish, the European cyprinid Leuuspius delineatus, T1tis threat is caused by
dn infctious pathog.n, a rosettelike infacellular eukaryotic parasitethat i6 a deadlt nonspecific agent,It is probably carried byhealthy Asian fish, and could decrea.se fish biodiversity in Europe, as well as having implications for

The stnbieak L. delineatLts, i6 the only representative of its genus and the only nestguarding fish among European q?rinids. Once widespread in Europe, in the past 40 years it has inexplicably declined' and is now on the EuroDean lirt ofthreatened freshwater fjshesr. By (ontrast, since its introduction in 196(l into Romanian ponds near the River

Danube, the Asian toprnouth gudgeon, P, porva, has spread rapidly throughout
Europe' and has focally .olncldedltith L. dcliheatui extinctionsn . In laborarory experiments (for methods, see supplementary information), we found that

it is difficuh to identifu fish populationr that Third, this pathogen

commercial aquaculture.

could pose a threat to the cons ation of

European fish diversity.
Rodolphe E, Gozlan', so Stephn

+!qk- l

the holdjrg water of P patra a.ted an ^s absolute inhibitor of s pawning for L. delixeafnJ (no eggs ploduced in P palrawater cofipared with 1,596! 840 in control, clean water), and caused a large increase in fish mortality (69 a 3% deaths in the treatmentgroup, comoared with l6!2yo 1 P <0.05, M^nt
Whitney U-test;4 experiments). These results were confirmed in a large natural outdoor pond, where L, delifieatus populations
aeclined,by 96yo .lt,er
th ree

phiegl-Hilakel ,

Felst*, Paul Martin+, MirhaelL. Kenl9 'Cntre for ology & Hydrolog, Winlrith Technology Centre, Dorchester, Dorst DT2 82D, UK

e-fiail: re8@ceh.ac.uk tDepadment of Biological Sciences, ldaho State University, Pocatello, ldah o 83209, US A

spawning seasons

(2002-04; Fig.
P

la) after being mixed lvith

Fllr|rrcl I D.cllna ol
popubdon In

ku..tpru, d.lln alw

hrtllrrl

pond rfiGr thc L(noduc{on ol Paaudoratboro pawa anllll,

latgc

aaaoclstrd pall'6g!'r,Sphaarolltcum dat tuaata. !, The ex.ct ma,rlmul}t liklihood slima{es (r.d bar6, showing r,e,m ,) fot L, delineatut popolalionr in (he aut$mn are shown for four y.ar8. Slarting populationi ir April of200l and .re shown a! blue bdrr: thre represnt 1.200 L, dellneatut in 2001 . 60lt L. delifleatut ^ad prcsm{ in a rnired popul^tion with 6tJ0 P, pareu of
20{12

rease of l3o/oln theyear (2001i Fig. I a). Spawnparra ^ftiaed in g lvas totafly inhibit ed in L. delineatus after P parva wds lnftodlu.ed. lVe found that the decline ir L. delineatus (cau5d try total inhibition ofspawning,loss of bodycondition, and death) thatresulted from sharing water vitb P parva was caused by an infectious organism, Histological findings ftom moribtnd L, delineatus rndicdted exlcnsive infection ofvisceral organs, including the reproductive tis6ues, with an obligat intracellular eukaryotic pathogen (Fig. lb; see also supplementary Information) similar to the leih rosette alentfipha e ro thr ( u m de st! u e 4i that ^l infects Chitlook salmon, Oncorhynchus

par%. desp\te anin

P.

beforc

CEFAS Weymouth Laboratory Weymouth, Dorst DT4 8UB, UK SCenterfor Fish Disease Research, Depa*ment oi \,4rc,obiolo8y. Oregon State U.1rvers(v CorvalLs, Oregon 97331'3804, U5A

l
2. 3.

L6dse, D. M. Trcnds Ecol. Erol.8,133-137 (1993).

Vande'Zarden,J
Naturc

M Cds5eldn,J.M &Ratnurten
11999).

LE

4$, 464-4ti

telek, A. fhe heshwatet fishes ol Eurcpe: lhrcotened f6hes

ol Euope Gozlan.
R.

(AULA, W ieebad en, 1987 ) E, Pind*, A C &5he11ey,l.l.nshBial.61,

298-300(200?)
5.

7.

Anselescu, N Ro,ronici Bul. Cctc. Pisc. tO, 99-109 (971). Wol1,af,'Wais, A., Wdtam, 6., Auer, B , Mikschi, E. & Hain, A. Hydtobialogia 409,123-129 (999). tuku5h,K D.,Mendoza,L.,Adkinlor, M.A.6 Hednck, R P ) Eukatyol Mictobial 50,43O- 438 Q0A3).
GiLrrca, R. &

tshawytscha, and Atlantic salmon, Salmo salat. The presence ofthis pathogen in L. delinea-

D.D:. Aqtot 4 9.61,181-1q7 8. Mendor.a h L & Alfush <24O4) 9. St-Hilate, 5 , Ribble, C., T6xler, 6., Da!ier, 1 & Kenl, M. L Dis. Atuot. Otg 45,1/3179 QOOI) 10. Gilad,A.el al. Dis. Aquot. Otg. 4a,16-1A8 QAA2)

introdu.d

ir

2002. b, High -pow.r ligh{

rn icrograph ofa s.ction o f a L. delineotusliver Therc fu a focus ofphagocyti. cell! (arrflr) containing conspicuoui.orinophilic rosette-like agenti (pinL). (Slide stained with haernatorylin

and eo6in; f cale bar, 50 micrornetrr.)

tas that had been exposed to holding {ater ftom P parva, and its absence in the source population and in th controigroup ( =20), was confirmed by polymerase chain raction amplification ofits DNA trsing primers 6pe' cific to a small segment ofthe ribosomdl DNA of S. destruens. The prevaler ce of the rosette02005 Naiure PublishingGroup

Supplemlrtary Infonn.tlon acto'npaiier lhl! comm!nica(ion on Nrr!re s w.b1 t.i. Competiot fin6r.ial ird.r.stst at cldt pai ro.e
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