Geographical spread of bacterial and fungal diseases of - OIE

Rev. sci. tech. Off. int. Epiz., 1996, 1 5 (2), 603-632

Geographical spread of bacterial and fungal diseases of crustaceans

DJ . ALDERMAN *

Summary: The author discusses the way in which bacterial and fungal diseases of crustaceans can be and have been transmitted via commercial movements of stocks. Two classic examples of such diseases are presented, namely gaffkaemia (a bacterial disease of marine lobsters) and crayfish plague (a fungal disease of freshwater crayfish). In both cases, there is ample evidence that much of the disease spread can be linked to the commercial movement of infected animals caught from infected wild stocks and transported over large distances for wholesale and retail. In the case of crayfish plague, much of the relentless spread of this disease through Europe for nearly 140 years can also be linked to the movement of contaminated fishing equipment without disinfection.

K E Y W O R D S : Aerococcus viridans - Aphanomyces astaci - Bacteria -Crayfish - Crayfish plague - Fungi - Lobster.

INTRODUCTION

N u m e r o u s e x a m p l e s can b e ci ted of the w a y in w h i c h bac ter ia l and fungal d iseases of c rus taceans h a v e b e e n spread b y c o m m e r c i a l m o v e m e n t s and t ransfers of the hos ts . Rather than p r o d u c i n g a list of the large n u m b e r of cases , this r e v i e w wi l l d i scuss in detail a s ingle major e x a m p l e of a bac ter ia l d i sease and one of a fungal d i sease . B o t h diseases are ' c l a s s i c ' d i seases of their type , and g o o d ev idence exis ts of the w a y in which these infect ions h a v e b e e n spread by c o m m e r c i a l m o v e m e n t s . T h e bac ter ia l disease is gaf fkaemia of lobs te rs and the fungal d i sease is crayfish p l ague .

BACTERIAL DISEASES: GAFFKAEMIA

Gaffkaemia is a bac ter ia l d i sease cons ide red pr imar i ly to b e of N o r t h A m e r i c a n origin, w h i c h is e n d e m i c in s tocks of Homarus americanus in A m e r i c a n wa te r s . However , ou tb reaks of infect ion in H. gammarus h a v e occur red regular ly in E u r o p e a n waters in recen t yea r s . M a n y of these ou tb reaks h a v e b e e n assoc ia ted w i t h the ho ld ing of impor ted s tocks of H. americanus in the s a m e faci l i t ies . S u c h impor t s s tar ted w i t h the d e v e l o p m e n t of t r ans -At lan t i c j e t aircraft, w h i c h m a d e the t ranspor t of such valuable, pe r i shab le ca rgoes e c o n o m i c and prac t ica l . T h e abil i ty to impor t lobs ters in

* Ministry of Agriculture, Fisheries and Food, Fish Diseases Laboratory, Weymouth, Dorset DT4 8UB, United Kingdom.

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this w a y has resul ted in the retail marke t of the Un i t ed K i n g d o m be ing suppl ied largely w i t h A m e r i c a n lobsters , w h i l e the h igher -va lue E u r o p e a n lobs ters are expor t ed to the rest of E u r o p e .

A n i m a l - t o - a n i m a l t r ansmiss ion of the p a t h o g e n Aerococcus viridans var. homari occur s on ly w h e n lobs ters are d a m a g e d in s o m e way , the w o u n d p rov id ing a suitable rou te of entry. H o w e v e r , c rus taceans he ld in in tens ive ho ld ing t anks do , all too often, have smal l l es ions w h i c h can p rov ide such an entry, even w h e n their c l a w s are banded to cont ro l the resul ts of aggress ion , ra ther than pegged , w h i c h causes m o r e d a m a g e . T h e cohabi ta t ion of local and impor t ed an imals , therefore , a l w a y s p resen t s a significant r isk of infect ion.

O n e specific case of the spread of gaffkaemia is represen ta t ive of the effects of the c o m m e r c i a l m o v e m e n t of infected lobs ters . D u r i n g a visi t to a lobs te r -ho ld ing site in nor thern Wales in 1978 , the m a n a g e r repor ted that a rapid mor ta l i ty of the lobs ter stock had started s o m e twenty- four hours previously . M i c r o s c o p i c examina t i on of a h a e m o l y m p h s a m p l e from m o r i b u n d lobsters s h o w e d the p re sence of character is t ic bac ter ia l te t rads in large n u m b e r s and thus p rov ided a p r e s u m p t i v e d iagnos i s of gaffkaemia, subsequent ly confi rmed by isolat ion of A. viridans f rom the an ima l s . The i m m e d i a t e p rob l em w a s conta ined by freezing the ent i re lobs ter s tock on si te, fo l lowed by full dis infect ion. Fur ther enqui ry revea led that the mor ta l i ty had b e g u n s o m e days after the in t roduct ion of a s tock of E u r o p e a n lobs ters f rom Ireland, and there was ev idence that this impor ted s tock h a d been in contac t w i th impor t ed A m e r i c a n lobsters . Howeve r , it w a s not poss ib le to confirm that suspic ion . Moreove r , immed ia t e ly before the nor th Wales mor ta l i ty had b e c o m e apparent , lobs ters f rom the Wel sh site h a d been expor ted to a who le sa l e site in the Ne the r l ands . In due course , a further gaffkaemia morta l i ty occur red on the Ne the r l ands site, affecting not only the lobs ters f rom north Wales , but also all o ther lobsters in that ho ld ing facility. T h e sugges ted transfer of gaffkaemia infect ion from one site to another by the c o m m e r c i a l t rade in lobs ters is i l lustrated in F igure 1.

S ince gaffkaemia is pr incipal ly a d i sease of lobsters , and A. viridans does not readily infect o ther decapods , such as c rabs , appropr ia te dis infect ion of s i tes that hold E u r o p e a n lobsters wi l l no rma l ly p reven t the es tab l i shment of infect ion in nearby wate rs . Howeve r , o ther decapods can b e infected (48) , bu t for such an imals , A. viridans is not rapidly lethal . Therefore , there is clearly a potent ia l r isk of creat ing a reservoir of infect ion in local c rus tacean s tocks in the i m m e d i a t e v ic in i ty of lobs ter -hold ing si tes, par t icular ly if those sites regular ly ho ld b o t h impor t ed and local s tocks . In addi t ion, A. viridans can b e isola ted f rom the m u d of infected ho ld ing ponds (15) . Desp i t e the regular impor t s of A m e r i c a n lobsters w h i c h h a v e taken p lace over m a n y years , it is still genera l ly be l ieved that, in the wa te r s of the U n i t e d K i n g d o m , gaffkaemia has no t yet b e c o m e es tabl ished as endemic . H o w e v e r , s o m e r e v i e w s now sugges t that this is no longer the case (47) .

FUNGAL DISEASES: CRAYFISH PLAGUE

Crayfish p l ague (krebspest, la peste) is undoub ted ly one of the b e s t - k n o w n , if not the bes t -known , d iseases of inver tebrates . T h e accumula ted l i terature of the d isease is n o w very ex tens ive ; s t re tching b a c k over 130 years to w h a t is be l i eved to b e the first record of its occur rence in E u r o p e , in nor thern Italy in 1865 . Affect ing only the

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F I G . 1

A n example of a commercial movement of gaffkaemia

freshwater crayfish, and l eav ing all o ther aqua t ic spec ies unaffected, crayfish p l a g u e has i m p r e s s e d obse rve r s and inves t iga tors th roughou t its history, b y its ex t r eme virulence for E u r o p e a n crayfish, the largest f reshwater inver tebra te of the E u r o p e a n continent .

Crayfish p l a g u e is a m y c o s i s , and the ae t io logic agent is an o o m y c e t e , Aphanomyces

astaci Sch ikora . A l t h o u g h in na ture it is k n o w n only as an obl iga te p a t h o g e n of the freshwater crayfish, A. astaci c an readi ly b e g r o w n in labora tory cul ture . U n e s t a m demons t ra ted that the fungus is c lear ly of N o r t h A m e r i c a n origin, and that all freshwater crayfish that h a v e been cha l lenged , o ther than those of N o r t h A m e r i c a n origin, are h ighly suscept ib le to infect ion wi th a le thal o u t c o m e (52 , 5 3 , 5 4 ) . T h e virulence of A. astaci to E u r o p e a n crayfish is a c lass ic e x a m p l e of the in t roduct ion of a d i sease-caus ing agent to a n e w area, resul t ing in the e x p o s u r e of na ïve popu la t ions of crayfish to an aggress ive p a t h o g e n (55) .

History of the spread of crayfish p lague in E u r o p e

A s U n e s t a m demons t r a t ed , the m a r k e d res i s tance of N o r t h A m e r i c a n crayfish species to A. astaci, and the suscept ib i l i ty of n o n - N o r t h A m e r i c a n spec ies , s t rongly suggest that A. astaci is a N o r t h A m e r i c a n o rgan i sm (52 , 5 3 , 54) . A. astaci and N o r t h A m e r i c a n crayfish appea r to h a v e a r easonab ly b a l a n c e d hos t -pa thogen re la t ionship in which dras t ic ep izoot ics are rare . Th i s con t ras t s s t rongly w i t h the u n b a l a n c e d destruct ion w r o u g h t by A. astaci in E u r o p e , the h is tory of w h i c h , desc r ibed be low, suggests s t rongly that A. astaci w a s in t roduced in to E u r o p e in the mid -n ine t een th century, p r e s u m a b l y on infected, N o r t h A m e r i c a n carr ier crayfish.

In m o d e r n t imes , the m o s t popu l a r A m e r i c a n crayfish spec ies for cu l tu re in E u r o p e has b e e n the s ignal crayfish (Pacifastacus leniusculus), w h i c h U n e s t a m and Weiss have s h o w n to b e infected in its na t ive e n v i r o n m e n t (56) , and w h i c h Pe r s son and

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Soderhä l l h a v e demons t r a t ed to b e a resis tant carr ier of crayfish p l a g u e (30). P. leniusculus, however , w a s not in t roduced into E u r o p e unt i l the mid- twen t ie th century, in a b id to rep lace popu la t ions of A. astacus des t royed by crayfish p lague . T h u s , a l though it has b e e n s h o w n to b e a vec tor in recent crayfish p l a g u e epizoot ics in E u r o p e (3) , the s ignal crayfish w a s clear ly not associa ted wi th the original in t roduct ion of crayfish p l ague m o r e than 120 years ago . A n o t h e r N o r t h A m e r i c a n crayfish, Orconectes limosus, h a d cer tainly b e e n in t roduced in to E u r o p e by 1 8 9 0 (58), bu t this w a s s o m e t ime after the first ind ispu tab le ou tb reaks of the d i sease . The r a inbow trout {Oncorhynchus mykiss), another Nor th A m e r i c a n spec ies in t roduced for aquacul tu re , m a y b e a potent ia l carr ier of crayfish p l ague ( 1 , 16) , bu t w a s not in t roduced into E u r o p e before 1879 , a few years after the first cases of crayfish p lague occur red . S o m e m o r e recent ou tbreaks , such as those in Spa in , m a y b e re la ted to the in t roduct ion of another Nor th A m e r i c a n crayfish, the Lou i s i ana s w a m p crayfish (Procambarus clarckii), w h i c h is n o w extens ive ly na tura l i sed in Spa in .

T h e sp read ing chain of crayfish p l ague mor ta l i t ies , w h i c h con t inues across Europe to this day, can b e t raced b a c k to the P la teau de Langre s b e t w e e n M o r v a n and Lorra ine in F rance , in 1874 . T h e r e is, however , an earl ier d iscrete series of crayfish morta l i t ies w h i c h m a y also h a v e b e e n due to crayfish p lague . T h e s e took p lace in Lombardy , nor the rn Italy, and b e g a n in the s u m m e r of 1859 , a l though earl ier mor ta l i t ies in the Sa rn ico reg ion of Italy m a y also b e re la ted (8) .

In the s u m m e r of 1859 , crayfish b e g a n to die in n u m b e r s in L o m b a r d y (Fig . 2) , and the affected area spread eas twards t owards the Veneto , r each ing G a m b a r a , I socel la and Verona in Sep t ember and the p rov inces of Veronese and Trev ig i ano by D e c e m b e r (8). In 1860, morta l i t ies w e r e repor ted near Bresc ia . Fur ther dea ths w e r e repor ted in r ivers of the Verona reg ion in the spr ing of 1 8 6 1 , inc lud ing the r iver B e n a c o . Eas t of the A d i g e , the wa te r s of Zev io , Pe r sacco , Palu , Valiese, Ra ldon , San G i o v a n n i Lupa to to , But tapie t ra , O p p e a n o , U p p e r M e n a g o and the B o n g i o v a n n i w e r e all affected, and in D e c e m b e r 1861 the first dead crayfish w e r e found in L a k e G a r d a (23) . To the w e s t of the A d i g e , the infect ion spread to Belfiore Diporc i le and B i o n d e , a m o n g o thers , and appeared in the U p p e r F ibbi lo , the An tane l lo and the Fossa Ba lb i , as w e l l as spread ing d o w n s t r e a m from the Fe r razze de San Mar t ino . T h e d isease a lso appea red in the Duga l Fonta ine , the Sarega , the L o w e r Tartoro and in the Cerea and Casa l eone va l l eys (23) . By D e c e m b e r of 1864, the d isease had reached the source of the r iver Si le at Casacorba (26) . In February 1865 , the infect ion spread further in the Si le and Bot ten iga ca tchments and then to the r ivers Storga, M e l m a , L i m b r a g a and M a g n a g o l a . By Apr i l of that year this d isease had infected the r ivers Muses t r e , Muses t re l l e , Pero , Vali lo and other lesser w a t e r w a y s (26) .

S o far, wr i t ten repor ts of morta l i t ies have been found only for s t r eams on the north s ide of the P o , but at that date , before the unification of Italy, the r iver fo rmed the b o u n d a r y of Aus t r i an territory. Pol i t ical boundar i e s m a y thus h a v e inf luenced any inves t igat ions or repor ts and therefore affected the apparent d is t r ibut ion of morta l i t ies .

T h e severity, extent and rapidi ty of spread of the mor ta l i ty ind ica tes an infect ious d isease and the only k n o w n crayfish d isease of such severi ty is crayfish p lague . However , there is no hard ev idence to support this hypo thes i s and this ser ies of ou tbreaks is separa te , physical ly and temporal ly , f rom the ma in cha in of sp read of crayfish p l ague in Eu rope . It w a s also sugges ted that these mor ta l i t i es co inc ided wi th the widesp read in t roduct ion of the use of copper su lphate in to v i t icul ture (11) . T h e r e h a v e been no m o r e crayfish p lague morta l i t ies repor ted from Italy, ei ther in the Po

F I G . 4

Crayfish plague in France and Italy in 1876

F I G . 5

Crayfish plague in France, Germany and Italy in 1877

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val ley or e l s ewhere , bu t the w a y in w h i c h the mor ta l i ty spread , as r epor ted by Ninni (26) , has all the character is t ics of p l ague . Certainly, Sch ikora w a s c o n v i n c e d that the I ta l ian mor ta l i t ies w e r e p l a g u e and repor ted that I taly h a d m a d e major efforts to res tock the r ivers of L o m b a r d y wi th crayfish ' shor t ly before her ent ry in to the w a r ' (p resumably the Firs t Wor ld War ) (45) . It is of interest that I taly is the only wes te rn E u r o p e a n count ry w h i c h has not apparent ly repor ted crayfish p l a g u e mor ta l i t i es since 1900 .

A l t h o u g h Sel igo repor ted that there w e r e crayfish mor ta l i t ies in the r iver Sp ree in nor thern G e r m a n y in 1864, he did no t be l i eve that these w e r e due to crayfish p lague (46) . If w e accept this view, then, the site of the first ep izoot ic in E u r o p e nor th of the A l p s appears to h a v e b e e n in F rance on the P la teau de L a n g r e s b e t w e e n M o r v a n and Lor ra ine in 1874-5 (Fig. 3) ( 3 3 , 58) .

T h e Pla teau de Langre s is the centra l wa te r shed b e t w e e n major r ivers such as the M e u s e , Se ine and R h i n e . Crayfish p l a g u e first appeared on this p l a t eau in 1874 . In the fo l lowing three years , infect ion appeared at a large n u m b e r of si tes a round the plateau, inc lud ing the sou thern N i è v r e and Jura depa r tmen t s , the no r the rn M e u r t h e and the Mose l l e , and in t r ibutar ies of the M e u s e , Rh ine , Se ine and S a ô n e r ivers (Fig . 4 ) . F r o m this focus , a re lent less sp read of morta l i ty b e g a n w h i c h h a s con t inued , w i t h only t empora ry remiss ions , to this day.

In 1877 , crayfish p l ague spread further into France , to the depa r tmen t s of A i sne , A u b e , H a u t e - M a r n e and Vosges (to the r iver Vair) (5) and, for the first t ime , morta l i t ies w e r e no ted in G e r m a n y in the vic ini ty of F rankfu r t - am-Main (Figs 5 and 6) (51) . The next year, in F rance (58) , mos t of the depa r tmen t of M e u s e , apar t f rom the r ivers Vinte and Lo iven , w a s infected before M a r c h . In the M a r n e depar tment , the Se ine basin r ivers and the region of Vitry le Franço is w e r e affected, in addi t ion to the rivers Marne , Cher, Viere , Bruxene l le , Ge rmene l l e and the M a r n e - R h i n e - S e i n e Cana l , as we l l as all Se ine tr ibutaries except the A m a n e e , Vanne , L a n d e o n and B r e v e n n e s . In addi t ion the A u b e , Lo ing , Fus in , Luna in , L a Bres le and A n d e l l e w e r e infected and crayfish p lague had also reached the R h ô n e bas in in the D o l e depar tment , v ia the L a Veyle tr ibutary of the S a ô n e and the Seran (a R h ô n e t r ibutary) .

In Germany , by M a r c h 1877 , the p l ague h a d appea red near S t ra sbourg and in A l sace . In July and Augus t , crayfish that had b e e n b rough t f rom the r iver H ü n s b r u k and the Eifel to M a i n z all d ied, sugges t ing that those source r ivers w e r e infected (Fig. 7) (20) . In Hessen -Darms tad t and Baden , crayfish w e r e first infected in the s u m m e r of 1878 .

Fur ther ex tens ions in France in 1879 inc luded the C o n e y in the Vosges , all t r ibutaries of the Se ine in the A i s n e depar tmen t and the r iver Thé ra in in the Oise depar tment . To the east, in Germany , p lague appeared in the M u n i c h reg ion in January and in Sep t ember an outbreak started in upper Aus t r ia : at G m u n d e n on L a k e Traun, in the K l a m b a c h at Gre in and in the K r e m s , wh i l e morta l i t ies w e r e repor ted to be spread ing a long the upper D a n u b e (Fig. 7) (5).

In 1880 , in southern Germany , crayfish died in the A l t m ü h l and its t r ibutar ies , inc lud ing the Wiese th and the Sulz , wh i l e in Be lg ium, L u x e m b o u r g and Al sace Lorra ine , morta l i t ies occurred in the r ivers Mose l l e , Saar, O r n e , Seille and N i e d (46) . T h e morta l i t ies in the D a n u b e spread downs t r eam and into t r ibutar ies in the Kulpa region on w h a t is n o w the Aus t r i an -S loven ian border reg ion (14) . A l l these ou tb reaks w e r e associa ted wi th the original P la teau de Langre s focus but , by the end of 1880,

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F I G . 6

The progress of crayfish plague in France, by department, from 1876 to 1890

mortal i t ies w e r e occu r r ing in nor the rn G e r m a n y (Fig . 8) , inc lud ing the Rorsee , Thuringia , M e c k l e n b u r g and S a x o n y and the B r a n d e n b u r g M a r k (20, 25 , 36 , 37 ) , and had b e g u n to sp read up the Mei t ze l f rom the O d e r (57) .

The fo l lowing year, 1 8 8 1 , infect ion r e a c h e d u p the R h i n e into Swi tze r l and at Be rne . In southern G e r m a n y and u p p e r Aus t r i a , in Oc tobe r and N o v e m b e r , crayfish mortali t ies w e r e repor ted f rom Wels and in the E i t e rbach (35) , as we l l as f rom the Tauber and t r ibutar ies of the M a i n (46) . To the east, F r a n k e repor ted further ex tens ions in the K u l p a reg ion , w h i c h a d v a n c e d into the headwa te r s of these s t r eams over the nex t three years (Fig . 9) (14) . O n c e crayfish p l a g u e h a d es tabl i shed itself in nor the rn Germany, m o r e a reas b e c a m e affected (Fig . 9) , w i th n e w ou tbreaks in the B o b e r in Silesia, in the K u d d o w in the O d e r reg ion , in the Fe rze and S c h w a r z w a s s e r in the Weichsel r eg ion of w e s t e r n Pruss ia and at A n g e r m u n d e in B r a n d e n b u r g (44, 4 6 ) .

In 1893 , the r iver A l t m ü h l lost all crayfish (6) , and there w e r e further mor ta l i t ies in the K u d d o w . To the nor th , the B r a h e of w e s t e r n Pruss ia w a s affected, as w e r e the waters of the K a m o n i c a , Z e m p l o n a , Widlgar tenf luss , Weichse l and Mischkerf le i ss (46). T h e u p l a n d a reas of the Gla tz p rov ince of Si les ia ( n o w the K l o d z k o distr ict of Poland) w e r e i nvaded u p the eas tern Gla tzer ( n o w N e i s s e ) (Fig . 9) .

In w h a t are n o w S loven ia and sou th Aus t r ia , b e t w e e n 1885 and 1890 (Fig . 10) , half of the r iver T e m n i c a w a s affected (14) , as w a s the Ljubl jana reg ion , and crayfish plague s tar ted a t en-year a d v a n c e u p the r iver G u r k and its t r ibutar ies . In w e s t e r n

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F I G . 7 F I G . 8

Crayfish plague in Europe in 1879 Crayfish plague in Europe in 1881

Pruss ia , the D r e w e n , Ossa and L iebe w e r e affected (46) , and the con t inu ing spread of infect ion in the east led to morta l i t ies in L a k e D o u b u z h i s in nor th -eas te rn La tv ia by 1886 (51) .

T h e year 1890 s aw further morta l i t ies in L a k e D r e w e n z and L a k e E w i n g in the Passer reg ion of wes t e rn Pruss ia . Ove r the nex t t w o years , major ou tb reaks of crayfish p l ague w e r e repor ted in Russ i a (Fig. 11), f rom the r iver L u g a in the St Pe tersburg region, from the Volga and from the L a k e O n e g a bas in (7) . In the ' r u s h i n g wa te r s of the Volga ' (to quote Sch ikora) , crayfish p lague cove red 3 ,000 k m to reach the Caspian Sea by the a u t u m n of 1892 (Fig. 11) (45) . T h e infect ions in the D a n u b e spread d o w n s t r e a m to reach the B lack Sea , and devas ta ted crayfish popu la t ions in the coastal p rov inces . A s for the D a n u b e t r ibutar ies , in format ion is on ly ava i lab le f rom the Kulpa region, w h e r e the infect ion had apparent ly spread th rough u n d e r g r o u n d s t r eams to the r iver Rinse . In wes te rn Pruss ia , the M a s u r e n w a s infected, as w e r e the w a t e r s around Shia laa i in central La tv ia (51) .

B y 1893 , in France , crayfish had comple te ly d i sappeared f rom Lor ra ine . In the Ku lpa region of the Ba lkans , the p l ague h a d spread to A t e n m a r k t . Crayfish p lague con t inued to spread th rough Russ ia and the Bal t i c s tates on a g rand scale . T h e Dniepr w a s infected d o w n to the rapids at Yekater inos lav (7) , w h e r e the pi les of dead crayfish p roduced such an unbearab le smel l that specia l efforts had to b e m a d e to b u r y them. In La tv ia the lakes and r ivers of the N i a m u n a s ( n o w N e m a n ) and Niar i s ( n o w Vilnia) bas ins w e r e affected, comple te ly eradica t ing crayfish in the w a t e r s of Ssv iachensk , Trakaisk , Ut iansk , Bi rzha i sk and Varniaisk (Fig. 12). Th i s rapid spread of the disease in La tv ia has b e e n at tr ibuted to the in t roduct ion of infected crayfishing equ ipment from G e r m a n y (51) . By 1894 the further spread of the d isease in the Bal t i c states b rough t infection to Kur l and ( n o w Cour land) in southern Latv ia , L ivon ia in nor thern Latv ia and Es ton ia (40) . In Russia , crayfish p lague spread to the r iver K l i a s ma , wh ich w a s a t r ibutary of the Volga, as w a s the Dv ina (in the Vi tebsk dis tr ict) , and also

New outbreak Already infected New outbreak Already infected

New outbreak

F I G . 11

Crayfish plague in Europe from 1890 to 1892

611

New outbreak Already infected New outbreak Already infected

F I G . 9

Crayfish plague in Europe in 1880

F I G . 10


Already infected

612

infected lakes in the V lad imi r distr ict (Fig . 12) (7) . T h e des t ruct ion of crayfish in R u s s i a n l akes and r ivers con t inued in 1 8 9 5 , w i th losses of s tocks in the r iver Beres ina (a t r ibutary of the Dn iep r ) , the M o s c o w river, the r iver O k a and lakes of the Suvalki district . In 1896 , losses occur red in the Scheksna in the Ja ros lav distr ict in Russ ia , the D u n a in Kur l and and E m b a c h in L ivon ia (7) . In nor thern G e r m a n y the l owland areas of the Gla tz reg ion w e r e affected, twe lve years after the first appea rance of crayfish p l ague in the up lands .

F I G . 1 2

Crayfish plague in Europe in 1 8 9 3

In 1897 , crayfish p l ague w a s affecting the Tchern igov and T v e r distr icts and lakes near Novgorod , in Russ ia . F r o m the Volga, p l ague w a s also sp read ing th rough the K a m a into the Ura l s , ' f rom w h e r e , ' wro te Schikora , ' i t w a s a smal l mat te r for it to reach the O b via the Tura and there in Siber ia to annihi la te the eas t e rnmos t crayfish co lon ies of the R u s s i a s ' (Fig. 13) (45) . In L ivon ia the r iver W o o , and L a k e Werro th rough w h i c h it flows, w e r e con tamina ted (19) . D u r i n g the nex t t w o years , crayfish p l ague reached the Pol tava, Kha rkov and Pskov distr icts of Russ i a (7) and the river A a , a mortal i ty w h i c h had evident ly spread ups t r eam from Latvia . In w h a t are n o w the Bal t ic s tates , the r iver D v i n a and L a k e Pe ipus (from the W o o ) had b e c o m e infected (7, 19). Howeve r , Tzukerz i s repor ts that, after 1902 , there w e r e no n e w outbreaks

613

F I G . 13


In 1 9 0 3 , Sch ikora , w h o w a s con t inu ing his inves t iga t ions , r epor ted ou tb reaks from the N a r i e n s e e (wes te rn G e r m a n y ) and M e c k l e n b u r g , and f rom Volhynia in Russ i a (42, 43 ) . In Bavar ia , n u m e r o u s ou tb reaks occu r red inc lud ing o n e in the r iver A u r a c h (49). In 1904 , in G e r m a n y , crayfish p l a g u e w a s identif ied in Z a n a h a u s e r See . T h e following spr ing , it had spread f rom a n e w focus in the N e u m a r k ( south-eas t of the Oder and sou th of P o m e r a n i a , and n o w in Po land ) , to the K l o p p s e e and the Mucklenburger See .

F in land h a d first b e e n infected in about 1900 (a l though few detai ls h a v e b e e n traced). In 1907 , the d isease r eached S w e d e n f rom F in land (Fig . 14) , w h e n impor t ed , infected crayfish w e r e found to b e m o r i b u n d on arr ival in S t o c k h o l m and w e r e jet t isoned into the h a r b o u r w h i c h lies at the en t rance to the M a l a r e n (4) . D e a t h s b e g a n the next year, w h e n the m o s t p roduc t i ve crayfish w a t e r s of S w e d e n , the M a l a r e n and Halmaren , w e r e des t royed . B y the end of 1908 , all the crayfish in the H a l m a r e n w e r e dead. T h e d isease had spread b e t w e e n the t w o lakes t h rough the r iver Esk i l s tunaâ , in which the crayfish also d ied (4) . Con t ro l s w e r e imposed , w h i c h succeeded in conf in ing

in Latvia for s o m e t ime (51) . In o ther infected r eg ions , w a t e r s that had p rev ious ly escaped crayfish p l a g u e b e c a m e affected, i nc lud ing the Pansdor fe r See in Si les ia (Fig . 13) (43) .

New outbreak Already Infected

614

F I G . 14


E l s e w h e r e , large mor ta l i t i es occur red in the U k e r m a r k reg ion of G e r m a n y from 1912 to 1914 and from 1923 to 1925 (38 , 39 ) , and in 1920, fo l lowing a per iod of near ly twen ty years in w h i c h there w a s litt le or n o spread of the d i sease in La tv ia , n e w ou tbreaks of crayfish p l a g u e w e r e repor ted in L a k e Obia la and L a k e D u s i a and in L i thuan ia (24 , 51) .

A re laxat ion of cont ro ls in S w e d e n in the late 1920s resu l ted in crayfish dea ths in 1928 in L a k e A d d a r in R o s e n g e n , in the lower r eaches of the Dalev, and in the east and wes t Go th i c ends of the G o t a Cana l , as we l l as in the major i ty of confluent lakes and s t reams (Fig . 15) (27) . T h e Tidern , Osan and Vikern lakes w e r e a lso affected. In 1929 , infect ion spread from the Go ta Cana l a rea to the r iver of S t aang A and Lake A s u n d . E l s e w h e r e in S w e d e n , crayfish dea ths occur red in Nashu l t a L a k e , in the A d d a r n in eas tern U p p l a n d , and in lakes and s t r eams in w e s t e r n Os te rgo t land . Lake Erken , the mos t p roduc t ive crayfish lake in S w e d e n , w a s devas ta ted b y crayfish p lague in 1 9 3 1 . T h e s e mor ta l i t i es l ed to major n e w s tudies b y Nybe l i n , w h i c h resu l ted in the first i sola t ion and cul ture of the pa thogen (27, 28 , 29) .

crayfish p l a g u e in S w e d e n to the lakes and r ivers of the H a l m a r e n and Mala ren sys tems (4) . D u r i n g th is pe r iod , howeve r , infect ion spread s teadi ly t h o u g h these wa te r s .

New outbreak Already infected

615

F I G . 15


The ou tb reak of the S e c o n d Wor ld War r educed the n u m b e r of easily t raceable reports of crayfish p l ague , a l though at least o n e further ou tb reak w a s no ted in 1943 in Latvia , in L a k e Shvimi l t i s (51) . Manns fe ld r e v i e w e d earl ier ou tb reaks in the Bal t i c states (22) , and the ser ies of ou tb reaks in the Ba l t i c r eg ion con t inued after the war , e.g. in Lakes Ga l s tas and Zaps i s in 1 9 5 1 , L a k e s Ungr i s , Gav i s , Sh lav inas , Sut r inas and Shiaksht ias in La tv ia in 1 9 6 0 - 6 3 and in L a k e Sp indz ius and the Traka i distr ict in Li thuania in 1 9 6 7 (24) . H o w e v e r , in 1956 , for the first t ime s ince crayfish p l a g u e h a d advanced in to S w e d e n in 1907 , a comple t e ly n e w area of E u r o p e w a s infected. It w a s the Iber ian pen insu la (Fig . 16) , w h e r e the first ou tb reaks appear to h a v e occur red in the r iver D u e r o in the Val ladol id reg ion (10) . A further large mor ta l i ty of crayfish occurred in Spa in in 1 9 6 5 , in the r iver U c e r o in the Sor ia distr ict . T h i s infect ion m a y have spread f rom Astacus leptodactylus that had b e e n in t roduced f rom G e r m a n y , a l though Aphanomyces w a s neve r pos i t ive ly identified (10) .

A further and p e r h a p s inevi tab le ex tens ion occur red in 1 9 7 1 w h e n crayfish p l a g u e was identified in N o r w a y for the first t ime . It appea red in t w o r ivers , bo th of w h i c h had their sources in N o r w a y bu t then f lowed ac ross the bo rde r in to S w e d e n (Fig . 16) . In the Vrangse lven , infect ion w a s de tec ted ve ry c lose to the b o r d e r in A u g u s t (17) . It then spread ups t r eam, despi te a t t empts to p reven t this b y u s i n g e lec t r ic fences (20 , 21) . The river Veska w a s also affected.


616

New outbreak

F I G . 16


T h e first pos i t ive identif icat ion of A. astaci in Spain w a s m a d e in 1978 from crayfish f rom the r iver R iaza (Fig . 17). T h e infect ion w a s be l i eved to h a v e or ig ina ted from i l legal ly impor t ed A. leptodactylus. Crayfish p l ague then spread to the r iver Guad iana in C i u d a d Rea l and to o ther r ivers in the region . Cuél lar and Col l record the con t inu ing spread of the d isease in Spain , t h roughou t 1979 (10) . In J u n e it infected the rivers C a d a g u a and Ba i rax y A y u g a in A lava . In July and Augus t , it spread to the rivers Ega , C i d a c o s , Araqu i l , Le i t za ran , E lorza , Salazar and Er ro y Lar ra ín in N a v a r r e ; the Guada lav ia r and J i loca y A l f a m b r a in Teruel , and the P isuerga in Valdol idad . In A u g u s t and Sep tember , Aphanomyces w a s identified in the Ebro and t r ibutar ies in Zaragoza , and in the I regua in L o g r o ñ o . Span ish crayfish morta l i t ies con t inued in M a y 1980 in the r ivers Júca r (Albace te p rov ince ) , Guad i ana (in Ciudad Real ) and G u a d a r r a m a (in Toledo) . T h e r e w e r e m o r e dea ths later in the Due ro r iver (in Z a m o r a ) , in Carr ion (Valencia) , in the B e r n e s g a (Léon) , and in E r e s e m a and Esgueva . (Val ladol id) . Mor ta l i t i es a lso occu r red in the w a t e r s of the Omec i l l o and A y u g a (Álava) , Ega , C idacos and Er ro (Navar re ) , I r egua (Logroño) , R iaza and Dura tón (Segov ia ) , Riaza and E s g u e v a (Burgos ) , Ja lón (Zaragoza) and in the Uce ro (Sor ia) .

Crayfish morta l i t ies still con t inued to occur in the ' o l d ' infected a reas s u c h as F in land , w h e r e W e s t m a n and N y l u n d repor ted on the spread of infect ion in the Pih la javes i wa te rway , w h i c h p rov ided a c lass ic case s tudy (59) .

Already infected

617

F I G . 1 7

Crayfish plague in Europe in 1 9 7 8

Fur ther ex tens ions of crayfish p l a g u e con t inued , w i t h the first suspec ted crayfish p lague mor ta l i t i e s in E n g l a n d b e i n g inves t iga ted in 1 9 8 1 (Fig . 18) . T h e subsequen t evolut ion of the infect ion in E n g l a n d and Wales is desc r ibed in m o r e detai l be low. T h e first ou tb reak of crayfish p l a g u e in G r e e c e w a s de tec ted in A u g u s t 1 9 8 2 (Fig. 18) (50) . It was init ial ly obse rved in the r iver K a l a m a s , i m m e d i a t e l y adjacent to a site to w h i c h 1,000 j u v e n i l e Pacifastacus leniusculus, impor t ed f rom a S w e d i s h hatchery , had b e e n int roduced in July. In 1983 a further ou tb reak w a s no ted in the nea rby river L o u r o s .

In late 1984 , the fishers of L a k e Civir i l , 2 0 0 k m east of Izmir in Turkey, repor ted abnormal i t ies on crayfish caugh t in the lake, and in the 1985 season they w e r e able to catch on ly 1 % to 5 % of the usua l quant i ty of crayfish (32) . T h e fishers f rom this lake w e r e left w i t h the cho i ce of su r render ing newly b o u g h t crayf ishing e q u i p m e n t or of m o v i n g to lakes wi th hea l thy s tocks . R a h e repor t s that they c lear ly did bo th , so that , by late a u t u m n 1985 , two o ther l akes w h i c h w e r e 100 k m to the east w e r e a lso showing s igns of crayfish p l a g u e (32) . By the 1986 season the m o s t impor t an t fishing lakes, Egridir , Sapanca , M a n y a s , U luaba t and Hirfanl i , w e r e found to b e infected and the fai lure of ca tches s h o w e d that 8 0 % of the Turk i sh crayfish s tocks w e r e a l ready affected b y the d isease (Fig . 18) . T h e p re sence of crayfish p roces s ing p lan ts on the most impor tan t l akes , Egr id i r and Uluaba t , w h i c h toge ther c o m p r i s e d 5 0 % of product ion , w a s r ega rded as one majo r r eason for the rapid sp read of d isease . A n o t h e r


618

F I G . 1 8

Crayfish plague in Europe from 1 9 8 0 to 1 9 9 5

cause w a s the free m o v e m e n t of fishers b e t w e e n the lakes , and the u s e of w o o d e n t ranspor t c ra tes w i thou t any dis infect ion m e a s u r e s . T h e or ig inal rou te by wh ich crayfish p l a g u e ar r ived in Turkey r ema ined u n d e t e r m i n e d (32) .

S o m e of the crayfish popu la t ions of the mid l and lakes of I re land fo rmed a n e w focus of crayfish p l a g u e (Fig. 18) (34) . T h e route by w h i c h the infect ion r e a c h e d Ireland could no t b e es tabl ished, a l though infected ang l ing e q u i p m e n t w a s suspec ted . N o further sp read of the d isease in I re land s e e m s to h a v e occu r red so far.

In 1990 , crayfish p l ague re turned to N o r w a y (Fig . 18) . A l t h o u g h the infect ion had p rev ious ly been found in t w o r ivers that c rossed the S w e d i s h border , the p l a g u e had b e e n con ta ined and e l imina ted by dis infect ing the r ivers (18) . Howeve r , in 1990 , the mos t ex tens ive r iver sys tem in Norway , the r iver Glomrna , b e c a m e infected, so that s imp le and dras t ic dis infect ion w a s no t a poss ib le op t ion .

T h i s final invas ion of N o r w a y comple t e s the l ong his tory of the spread of crayfish p l a g u e in E u r o p e . In t ime , every count ry on the cont inent h a d b e c o m e infected by A. astaci. M u c h of the in format ion on crayfish p l ague , par t icular ly in the per iod from 1880 to 1920, i s a c c o m p a n i e d b y c o m m e n t s about the ro le p l ayed b y commerc i a l crayfish t rappers and who lesa l e r s in the spread of the d isease . Scl i ikora d i scussed the ro le of c o m m e r c i a l m o v e m e n t s in some detail in h i s r e v i e w enti t led ' 5 0 yea r s of


619

crayfish p l a g u e ' (45) . H e w a s in n o doub t that it w a s p r e d o m i n a n t l y the w h o l e s a l e crayfish t rade w h i c h had taken crayfish p l a g u e f rom the or ig inal P la teau d e L a n g r e s focus to Ber l in in t he nor th of G e r m a n y , and to M u n i c h in the sou th , and then continued to impor t infected crayfish, b o t h to s tock w a t e r w a y s and to sell for food. T h e spread of p l ague e a s t w a r d s f rom G e r m a n y has b e e n a t t r ibuted to the in t roduc t ion of infected crayf ishing e q u i p m e n t and the act ivi t ies of m o b i l e crayfish ca tchers in Russ ia , who m o v e d f rom r iver to l ake to r iver (7 , 51 ) . M u c h the s a m e th ing appea r s to h a v e occurred near ly 100 years later in Turkey, w i t h exact ly the s a m e effect: a rap id and devasta t ing spread of infect ion (32) .

S o m e G e r m a n crayfish w h o l e s a l e r s had d e v e l o p e d e n o u g h exper t i se to r ecogn i se infected s tocks and to p lay a ro le in a t t empt ing to restrict the spread of infect ion (45) . Others w e r e m u c h less careful . T h e lack of sufficient disease-free s tock to satisfy the German m a r k e t caused a ma jo r p r o b l e m . W i t h o u t impor t s the who le sa l e r s w e r e u n a b l e to cont inue in bus ines s . Yet con t inued impor t s b r o u g h t w i t h t h e m the cer ta in ty that some of the i m p o r t e d crayfish w o u l d b e infected, and w o u l d con t inue to rep len i sh infections in G e r m a n w a t e r s . T h e e c o n o m i c re turns for ind i sc r imina te i m p o r t s of crayfish w e r e c lear ly a t t rac t ive . Repor t s of i l legal impor ta t ions inc luded cases in w h i c h crayfish w e r e b r o u g h t in in r u c k s a c k s or as h a n d luggage , and then ' sen t on in land as postal p a c k e t s as s tock ing crayf ish ' (45) . Para l le l s w i t h m o d e r n i l legal m o v e m e n t s of coldwater o r n a m e n t a l fish can b e d r a w n only too easily.

Severa l a t t empts w e r e m a d e to res tock wa te r s , s o m e t i m e s wi th shor t - te rm success . Crayfish re leased in to the M a i n w e r e th r iv ing in 1892 (41) . In contras t , the infect ion was still p re sen t in the A l t m ü h l in 1 8 9 3 , w h e r e in t roduced an imal s d ied rapidly (6). In 1894 in L a k e Boe th in , w h e r e crayfish h a d b e g u n to r epopu la te natural ly, a further mortal i ty occur red (40) . S imi la r ly in the N ü r n b e r g area, in the r iver Se lbe , a popu la t ion which had re -es tab l i shed itself w a s aga in des t royed .

A s m e n t i o n e d above , Sch iko ra repor ted that I taly had m a d e ' ene rge t i c ' a t t empts to restock the r ivers of L o m b a r d y (des t royed b y crayfish p l a g u e in the 1860s) (45) . T h e s e at tempts w e r e ha l ted b y the Firs t Wor ld War and by ' s u b s e q u e n t e c o n o m i c w e a k n e s s ' . The s a m e author repor ted that a F rench ' C o m m i s s i o n for the repopu la t ion of the r ivers in the r a v a g e d a r e a s ' w a s es tabl i shed in the Rh ine land , and had app roached a Ber l in wholesa ler for 100 ,000 res tock ing crayfish. Th i s reques t w a s refused, apparen t ly par t ly for ' pa t r io t i c ' r ea sons ( the Saa r l and w a s occup ied ) , and par t ly for c o m m e r c i a l r easons . Whether d isease-f ree crayfish cou ld h a v e b e e n ob ta ined in such n u m b e r s for such a purpose is uncer ta in .

In the mid - twen t i e th century, a n e w p h a s e of c o m m e r c i a l t ransfers of crayfish began , with the d e v e l o p m e n t of p r o g r a m m e s to res tock w a t e r s w i t h crayfish (again) , and to farm them. T h e s e n e w act ivi t ies h a v e invo lved the spread of the s igna l crayfish (P. leniusculus), and the s w a m p crayfish (Procambarus clarckii). T h e in t roduc t ion of the s ignal crayfish h a s b e e n s t rongly l inked w i t h severa l of the m o s t recen t sp reads of infection, i nc lud ing G r e e c e and Grea t Br i ta in .

Crayfish p lague in the Bri t i sh Isles

T h e first p r o v e n cases of crayfish p l a g u e in the Br i t i sh Is les da te f rom the ear ly 1980s, bu t there a re sugges t ions f rom the b e g i n n i n g of the twent ie th cen tury that crayfish p l a g u e m i g h t h a v e ar r ived in Br i ta in t owards t he end of its init ial sp read through E u r o p e . T h e r eco rded mor ta l i ty appears to h a v e s tar ted in about 1892 , on the

620

T h a m e s at S ta ines , and spread ups t ream, resul t ing in ' t he a lmos t c o m p l e t e des t ruct ion of the crayfish ... u n d e r s o m e of the m o s t c losely perfora ted b a n k s they lay l ike a red fr inge a long the r ivers ide u n d e r the w a t e r ' (9) . Th i s descr ip t ion cer ta inly s o u n d s like the effects of crayfish p l ague and the mor ta l i ty is desc r ibed as b e i n g ' d u e to a d i sease ' . Howeve r , the descr ip t ion of the w a y in w h i c h the crayfish died: ' t h e nea t little fresh wa t e r lobs ters turned a lmos t as red as if they had b e e n boi led , c rawled out of their ho les and d i ed ' (if correc t ly repor ted by Corn i sh , w h o appears to h a v e been a careful obse rve r ) , does no t agree w i t h w h a t actual ly h a p p e n s in an ou tb reak of crayfish p lague . Poss ib ly the crayfish p l a g u e mor ta l i t ies that had b e e n repor ted from m u c h of Europe dur ing the p rev ious 2 0 years inf luenced the in terpre ta t ion. Clearly, popu la t ions in the T h a m e s va l ley re -es tab l i shed quickly, as later on, in the 1930s , there w e r e other inves t iga t ions in to crayfish mor ta l i t i es in T h a m e s t r ibutar ies and s t r eams in the vicinity of Oxford (12 , 13) . Th i s rapid re -es tab l i shment fo rms a c lear cont ras t to the si tuation in E u r o p e a n r ivers w h e r e the p lague had s t ruck. F r o m the l imi ted pub l i shed details ava i lab le on the 1930s mor ta l i t ies , the an ima l s f rom the affected si tes appea r to have b e e n infected wi th The lohan ia contejeani, a wide ly dis t r ibuted mic rospo r id i an parasi te of crayfish w h i c h causes an i l lness k n o w n as porce la in d i sease . Porce la in d isease does not p r o d u c e m a s s or rapid mor ta l i t ies .

A further s ea rch for crayfish p l ague in E n g l a n d w a s p r o m p t e d by an enqui ry from Aus t ra l i a for crayfish d isease- infected an imals for potent ia l use as a b io log ica l control of crayfish in Aus t ra l i a (31) . In v i e w of the a l ready we l l -desc r ibed and wel l -publ i shed , seven ty -year h is tory of crayfish p l a g u e disasters in E u r o p e , one is d r iven to wonder at the a t t i tude of those invo lved in this ep i sode . For tuna te ly (in v i e w of the es tabl ished sensi t ivi ty of Aus t ra l i an crayfish to A. astaci), the inves t iga tors did no t find any an imal s infected w i t h crayfish p l ague and no a t tempt to obta in p lague- in fec ted animals f rom cont inen ta l E u r o p e s e e m s to h a v e b e e n m a d e .

T h e avai lab le ev idence argues s t rongly against the occur rence of crayfish p l ague in the Br i t i sh Is les before the m i d - 1 9 7 0 s . Such ev idence inc ludes the lack of any descr ip t ion of a p lague- l ike mor ta l i ty in na t ive crayfish s tocks , in cont ras t to the ' t o r ren t ' of publ ica t ions f rom cont inenta l E u r o p e , p lus the p re sence of good s tocks of crayfish before 1980 in every wa te r shed in E n g l a n d and Wales in w h i c h there were favourab le env i ronmen ta l condi t ions . H o w e v e r , the ques t ion of w h e t h e r crayfish p l a g u e h a s b e e n in the U n i t e d K i n g d o m s ince 1892 can neve r b e answered conclus ive ly . Th i s is b e c a u s e it w a s never scientifically es tab l i shed that crayfish p lague w a s p resen t in these w a t e r s before the 1980s . Equal ly , the absence of crayfish p lague - a nega t ive — w o u l d be imposs ib le to es tabl ish b e y o n d all doubt . Neve r the l e s s , it is clear that before 1980 the Bri t ish Is les had good s tocks of na t ive crayfish, and from 1 9 8 1 o n w a r d s , a ser ies of ou tb reaks that h a v e b e e n p r o v e n to b e crayfish p l a g u e has spread rapidly th rough E n g l a n d and Wales .

In genera l , crayfish h a v e not fo rmed a significant na tura l fishery in E n g l a n d or Wales . T h u s , there has neve r b e e n that s a m e e c o n o m i c i m p e t u s that , in France , G e r m a n y and Russ ia , p r o m p t e d the extens ive m o v e m e n t s of crayfish descr ibed above , w h i c h w e r e c lear ly respons ib le for mos t , if not all, of the spread of crayfish p l ague in con t inen ta l E u r o p e .

T h e first significant in t roduc t ion of exot ic crayfish into the Br i t i sh Is les w a s of the s ignal crayfish (P. leniusculus) in the per iod from 1976 o n w a r d s . In S w e d e n , the signal crayfish is es tabl ished as a carrier of crayfish p lague , and in its na t ive r ange in Cal i fornia it is subject to p l ague morta l i t ies . A l though the major i ty of s tocks impor ted

621

into the U n i t e d K i n g d o m c a m e f rom ha tche ry sou rces w h i c h t ook p recau t ions aga ins t disease t r ansmiss ion , s o m e , at least , are be l i eved to h a v e c o m e direct ly f rom N o r t h Amer ica . A s there w e r e n o checks on the hea l th s ta tus of crayfish impor t s in to the United K i n g d o m , the poss ibi l i ty that f a rmed s ignal crayfish in t roduced crayfish p l a g u e into the Bri t ish Is les canno t b e p roven , a l though the p rox imi ty in t iming b e t w e e n the introduct ion of s igna l crayfish f a rming in E n g l a n d and the c o m m e n c e m e n t of p l a g u e outbreaks is clear.

It is a lso c lear that there h a v e been m a n y in t roduc t ions of s ignal crayfish into fish farms and 'crayf ish f a r m ' s i tes t h roughou t E n g l a n d and Wales , and s o m e of these h a v e resulted in e scapes to the wi ld , w h i c h h a v e caused the es t ab l i shment of na tura l i sed popula t ions .

In the major i ty of cases of crayfish p l a g u e ou tb reaks in E n g l a n d and Wales over the last twe lve years , s ignal crayfish h a v e b e e n no ted to b e in c lose p rox imi ty to the infection si te. Admi t t ed ly , the ev idence for the p re sence of the s ignal crayfish has not always b e e n firmly es tab l i shed . H o w e v e r , only in o n e or t w o cases is there n o l ink wi th the poss ib le p rox imi ty of s ignal crayfish. A p a r t f rom one case descr ibed later, it has not been poss ib le to ob ta in s a m p l e s of suspec t s ignal crayfish, to confirm the carr ier status of those popu la t ions . S igna l crayfish from grave l pi ts nea r R i n g w o o d , Dorse t , have also b e e n found to b e carr iers of crayfish p l a g u e ( D J . A l d e r m a n , unpub l i shed findings).

S o m e natura l i sed popu la t ions of s ignal crayfish in Eng land are ev ident ly not carr iers of p lague , s ince they h a v e co-ex i s ted in the s a m e wa te r s as na t ive crayfish for m o r e than five years , w i thou t any ev idence of p l ague in the suscept ib le s tock, e.g. in the B y Brook and St. Ca the r ine ' s B r o o k in A v o n (M. Fray l ing , unpub l i shed findings).

The first ou tb reaks of crayfish p l a g u e appea r to have s tar ted m o r e or less s imul taneous ly in t w o r iver s y s t e m s in sou the rn E n g l a n d (Fig . 19) . In the s u m m e r of 1981, crayfish mor ta l i t ies w e r e repor ted from the r iver L e e at Ware L o c k and in the Sherston b r a n c h of the Br is to l A v o n at Eas ton Grey. Bo th r ivers h a d large popu la t ions of crayfish and the effects w e r e d r a m a t i c wi th the r iver b e d s b e i n g s t r ewn wi th dead crayfish. N o crayfish su rv ived d o w n s t r e a m of the mor ta l i ty s i tes and, in the fo l lowing months , mor ta l i t ies spread u p s t r e a m f rom the conf luences in t r ibutar ies such as the Tetbury A v o n and the R ib and B e a n e . A. astaci w a s isola ted in crayfish f rom these mortal i t ies (2) .

In the s u m m e r of 1 9 8 3 , further crayfish mor ta l i t i es occur red in the T h a m e s ca tchment area. T h e e v i d e n c e of such crayfish mor ta l i t i es is essent ia l ly ephemera l , since exoske le ta l r ema ins su rv ive for only a few w e e k s , even at w in te r wa t e r tempera tures . T h e d i s appea rance of crayfish f rom the r iver B l a c k w a t e r in Sur rey in the s u m m e r of 1 9 8 2 left n o r e m a i n s w h i c h cou ld b e inves t iga ted (Fig . 20 ) , bu t the mortal i ty in the nea rby r iver Wey in S e p t e m b e r 1983 w a s repor ted at a ve ry ear ly s tage (Fig. 21) . D e a d and dy ing an ima l s w e r e ob ta ined and isola tes of A. astaci w e r e m a d e , confirming that crayfish p l a g u e w a s respons ib le (2) .

In M a r c h 1984 , a mor ta l i ty w a s repor ted f rom the uppe r r eaches of the H a m p s h i r e Avon (Fig . 22) . It w a s conf i rmed to b e crayfish p l a g u e and, in less than three w e e k s , no crayfish w e r e left a l ive in the 4 0 mi l e s (80 k m ) of river. M o r e crayfish w e r e dy ing as a band of mor ta l i ty b e g a n to m o v e up the major t r ibutar ies f rom their conf luence with the A v o n . T h e d i s appea rance of crayfish from the r iver K e n n e t w a s comple t e ly unobserved at the t ime , be ing r ecogn i sed on ly later that s u m m e r , and a l though the on ly

F I G . 19

Crayfish plague outbreaks in England and Wales in 1981

New outbreak

F I G . 20


622

Mew outbreak

Already Infected

River Wey

New outbreak LZ] Already Infected

F I G . 21


F I G . 22

Crayfish plague in England and Wales in March 1984

624

p robab le cause w a s p l ague , there is lit t le proof. Similar ly , by that s tage , na t ive crayfish w e r e n o longer to b e found in the Dorse t F r o m e and the S tour (Fig . 23) .

P l a g u e w a s nex t conf i rmed to the w e s t of L o n d o n , in t r ibutar ies of the r iver Colne , inc lud ing the M i s s b o u r n e , in 1985 , and then to the south-eas t , in the r iver Daren th , in 1986 (Fig . 24) . In 1987 , a smal l s t r eam (the D o w l e s B r o o k ) in the Fores t of W y r e , wel l a w a y f rom the infected w a t e r s of sou the rn Eng land , w a s found to b e con tamina ted (Fig . 25) . A n es tabl i shed popu la t ion of s ignal crayfish w a s found in a p o n d wi th in the infected area, w h i c h w a s itself wi th in a na ture rese rve . T h i s mor ta l i ty effectively exposed any crayfish in the lower Seve rn w a t e r s h e d to crayfish p l ague .

N o n e w cases w e r e repor ted in 1988 or 1989 , bu t 1990 p r o d u c e d majo r new ex tens ions of crayfish p l ague . In the spr ing , several t r ibutar ies of the Br is to l Avon , in w h i c h na t ive crayfish h a d surv ived despi te the infect ion of the ma in r iver s ince 1981 , w e r e affected. T h e s e inc luded the B y B r o o k to the no r th of the Avon , and the Somerse t F r o m e and its tr ibutary, the Me l l s river, to the south (Fig . 26) . Fie ld inves t iga t ions s h o w e d that the mor ta l i ty in the r iver Me l l s had clear ly s tar ted in the head -wa te r s of the M e l l s , ra ther than ex t end ing u p s t r e a m f rom the m a i n river, Avon , s ince the animals in all par ts of the r iver died s imul taneous ly . Crayfish popu la t ions still su rv ive in a few side s t r eams (M. Fray l ing , pe r sona l c o m m u n i c a t i o n ) . In the Eas t M i d l a n d s , morta l i t ies f rom the r iver Ise , w h i c h is a t r ibutary of the r iver N e n e , w e r e conf i rmed to b e crayfish p l ague in Ju ly 1990 (Fig . 26) , and in A u g u s t the r iver C a m l a d , a t r ibutary of the upper Severn , w a s found to be infected (Fig . 26) . In M a y 1990 , repor t s of crayfish deaths in s ide s t r eams of the r iver W y e in Herefordsh i re could no t b e conf i rmed, bu t samples co l lec ted f rom the r iver A r r o w in Sep t ember w e r e p r o v e n to b e crayfish p lague (Fig. 26 ) . T h e mor ta l i ty in the r iver A r r o w appeared to h a v e b e g u n in the vic ini ty of a finfish farm, w h e r e s ignal crayfish (P. leniusculus) had b e e n in t roduced , bu t no examina t ion of these an imals w a s m a d e . R u m o u r s of s ignal crayfish in t roduced into the vic ini ty of the r iver C a m l a d cou ld not b e conf i rmed. T h e r e m a i n i n g major tr ibutary to the r iver Severn f rom the Wel sh borders , the r iver Clun , also appears to h a v e lost crayfish in 1992 , though this w e n t un reco rded (R. Gardner , pe r sona l c o m m u n i c a t i o n ) , and a conf i rmed isolate w a s m a d e from the Clun in 1995 .

Th i s sp read of the d isease in 1990 m e a n t that all major crayf ish-bear ing river sy s t ems south of the Trent w e r e infected by crayfish p l ague . A further major n o r t h w a r d s ex tens ion is be l i eved to h a v e occur red in M a r c h 1 9 9 1 , w h e n crayfish mor ta l i t i es w e r e repor ted b e l o w Bux ton in the r iver W y e (Derbysh i re ) . T h e fo l lowing A u g u s t , further mor ta l i t ies w e r e be ing repor ted in the m a i n r iver D e r w e n t , ups t ream of its conf luence wi th the B u x t o n W y e (Fig. 27) . Unfor tunate ly , no s ample s were col lec ted , so that the cause of these morta l i t ies r ema ins unconf i rmed, a l though further mor ta l i t i es in s ide s t r eams have occurred s ince .

In 1992 , the upper T h a m e s and s o m e smal ler southern r iver c a t c h m e n t s still re ta ined crayfish popu la t ions , bu t con t inu ing eros ion of these surv iv ing popu la t ions is to be expec ted , as occur red in nor thern E u r o p e dur ing the 1930s and 1940s (40) . An e x a m p l e of this e ros ion h a p p e n e d in January 1992 , w h e n the smal l T h a m e s tr ibutary ca t chmen t of the H i g h W y c o m b e W y e and W y c o m b e D y k e w a s infected (Fig . 28) .

T h e s teady spread of crayfish p lague in crayfish popu la t ions in E n g l a n d and Wales f rom 1980 o n w a r d s can often, in one w a y or another , b e associa ted wi th the in t roduc t ion of s ignal crayfish (P. leniusculus) into the i m m e d i a t e area for crayfish fa rming . It has not been poss ib le to examine these farm popu la t ions , w h i c h m u s t be suspec ted to b e carr iers of the infect ion. However , w h e n a c o m m e r c i a l s tock of signal

625


F I G . 23

Unconfirmed crayfish plague in England and Wales in 1984

New outbreak A$ready Infected

F I G . 24


626

F I G . 2 5


New outbreak [ZI Already

F I G . 2 6


6 2 7

New outbreak LZ! Already infected

F I G . 27

Crayfish plague mortalities in England and Wales in 1991


F I G . 28

Crayfish plague mortalities in England and Wales in 1992

628

crayfish w a s in t roduced into t anks of Austropotamobius pallipes at the Univers i ty of No t t i ngham, and a mor ta l i ty ensued , it w a s poss ib le to d e m o n s t r a t e a carr ier infection wi th A. astaci (3) . Clearly, therefore , at least s o m e s tocks of f a r m e d s ignal crayfish in Great Bri ta in are infected w i t h crayfish p l ague . T h e spread of crayfish p l a g u e in E n g l a n d and Wales dur ing the last fifteen years w o u l d s e e m to be c lear ly associated wi th the c o m m e r c i a l in t roduct ion and m o v e m e n t of infected, d isease-res is tant , carrier crayfish - ra ther than as a result of the m o v e m e n t of infected, suscept ib le crayfish to res tock w a t e r w a y s and sell for food, and of con t amina t ed crayf ishing equ ipmen t , as occur red th roughou t con t inen ta l E u r o p e m o r e t h a n a cen tu ry earl ier .

CONCLUSION

T h e his tor ies of bo th crayfish p l ague and gaffkaemia clear ly s h o w the haza rds of c o m m e r c i a l m o v e m e n t s of aqua t ic o rgan i sms w h e r e d isease is conce rned . T h e results, however , h a v e b e e n s o m e w h a t different. Crayfish p l a g u e h a s sp read remorse less ly across E u r o p e over a per iod of m o r e than 130 years to infect every country, p r e sumab ly as a result of l imi ted early in t roduc t ions of exo t ic crayfish, and replenished by further in t roduc t ions of o ther exot ic crayfish spec ies m a n y years later. T h e initial in t roduc t ions w e r e pe rhaps m a d e poss ib le by the arr ival of s t eamsh ips on the North At lan t ic c ross ing , enab l ing the transfer of smal l n u m b e r s of crayfish. O n c e the disease w a s es tabl ished in E u r o p e a n wate r s , the no rma l p roce s se s of t rad ing in crayfish for food and for s tock ing pu rposes , p lus the m o v e m e n t of crayfish t rapp ing equ ipment f rom one area to another , p roduced an inevi table c o n s e q u e n c e for the popu la t ions of suscept ib le crayfish in Eu rope . Th i s p rocess m a y b e clear ly con t ras ted w i t h the p rogress of gaffkaemia. Impor t s of A m e r i c a n lobs ters , at least in any significant quant i t ies , did not occur unti l the age of je t aircraft, w h i c h cou ld t ranspor t such h igh-va lue , per i shable cargoes economica l ly . La rge t o n n a g e s of potent ia l carr iers of gaffkaemia h a v e b e e n impor t ed repeatedly , and ye t these have , s o far, resul ted in relat ively only a few ou tbreaks of cl inical d isease . Moreove r , there is , as yet , no conc lus ive ev idence that gaffkaemia has b e c o m e pe rmanen t ly es tab l i shed in European lobster s tocks .

*

EXTENSION GÉOGRAPHIQUE DES M A L A D I E S B A C T É R I E N N E S ET FONGIQUES DES CRUSTACÉS. - D.J. Alderman.

Résumé : L'auteur montre comment les maladies bactériennes et fongiques des crustacés peuvent se transmettre à l'occasion de déplacements liés au commerce de ces espèces. Il prend deux exemples classiques de ce type de maladie : l'infection par Aerococcus viridans affectant les homards de mer, et la peste des écrevisses (une mycose affectant les espèces d'eau douce). Il existe de nombreuses preuves que, dans les deux cas, la propagation de la maladie est en grande partie imputable aux transferts commerciaux d'individus infectés, provenant de populations elles-mêmes infectées, et transportés sur de longues distances à l'occasion du commerce de gros et de détail. Dans le cas de la peste des écrevisses, l'extension inexorable de cette maladie en Europe depuis près de 140 ans peut être également liée à l'utilisation, sans désinfection, de matériel de pêche contaminé.

629

M O T S - C L É S : Aerococcus viridans - Aphanomyces astaci - Bactéries -Champignons - Écrevisse - Homard - Peste des écrevisses.

*

DISPERSION G E O G R Á F I C A D E E N F E R M E D A D E S B A C T E R I A N A S Y FÚNGICAS DE LOS C R U S T Á C E O S . - D.J. Alderman.

Resumen: El autor examina la forma en la que ciertas enfermedades bacterianas y fúngicas de los crustáceos pueden y han podido propagarse gracias al traslado de poblaciones con fines comerciales. Se presentan dos ejemplos clásicos de tales enfermedades: la enfermedad bacteriana de la langosta de mar causada por Aerococcus viridans y la plaga del cangrejo de río. En ambos casos existen sobradas evidencias de que la propagación de estas enfermedades está muy ligada al movimiento comercial de animales infectados, capturados en el seno de poblaciones salvajes infectadas y desplazados a larga distancia para su venta al por mayor o al detalle. En el caso de la plaga del cangrejo de río, la imparable extensión de esta enfermedad a través de Europa durante cerca de 140 años obedece en gran parte al movimiento, sin previa desinfección, de artículos de pesca contaminados.

P A L A B R A S CLAVE: Aerococcus vir idans - Aphanomyces astaci -Bacterias - Cangrejo de río - Hongos - Langosta - Plaga del cangrejo de río.

* *

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Geographical spread of bacterial and fungal diseases of - OIE