How Is Epizootic Ulcerative Syndrome (EUS) Diagnosed? 10

Food and Agriculture Organization of the United Nations

What you need to know about EPIZOOTIC ULCERATIVE SYNDROME (EUS) An extension brochure for Africa he designations employed and the presentation of material in this information Tproduct do not imply the expression of any opinion whatsoever on the part of the Food and Agriculture Organization of the United Nations (FAO) concerning the legal or development status of any country, territory, city or area or of its authorities, or concerning the delimitation of its frontiers or boundaries. The mention of specific companies or products of manufacturers, whether or not these have been patented, does not imply that these have been endorsed or recommended by FAO in preference to others of a similar nature that are not mentioned.

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Viale delle Terme di Caracalla, 00153 Rome, Italy or by e-mail to: [email protected] © FAO 2020 , Philippine isolates,1999 ©FAO/M.B. Reantaso ©FAO/M.B. sporangia , Philippine isolates,1999 Aphanomyces

Design and layout: José Luis Castilla Civit What you need to know about EPIZOOTIC ULCERATIVE SYNDROME (EUS) An extension brochure for Africa

Food and Agriculture Organization of the United Nations Rome, 2020 iii Required citation: FAO. 2020. What you need to know about epizootic ulcerative syndrome (EUS) – An extension brochure for Africa. Rome.

The designations employed and the presentation of material in this information product do not imply the expression of any opinion whatsoever on the part of the Food and Agriculture Organization of the United Nations (FAO) concerning the legal or development status of any country, territory, city or area or of its authorities, or concerning the delimitation of its frontiers or boundaries. The mention of specific companies or products of manufacturers, whether or not these have been patented, does not imply that these have been endorsed or recommended by FAO in preference to others of a similar nature that are not mentioned.

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Cover photographs: ©FAO/D. Huchzermeyer, Rhodes University. Preparation of this document

his extension brochure – What you need to know about epizootic ulcerative Tsyndrome (EUS) – provides simple facts or answers to frequently asked questions about EUS. This brochure is intended to address a wide range of audience from fish farmers and fishermen to extension officers as well as policy- makers as a public information campaign to make available factual information about the disease so that awareness may be raised for better understanding of its potential impact.

The original brochure, an outcome of FAO’s Technical Cooperation Project TCP/RAF/3111 Emergency Assistance to Combat Epizootic Ulcerative Syndrome in the Chobe/Zambezi River System, was prepared under the technical supervision of Dr Melba B. Reantaso (FAO) and Dr Rohana P. Subasinghe (FAO retiree).

The current version of the extension brochure is focused on Africa. This was prepared by Dr Melba Reantaso and Dr David Huchzermeyer (South Africa).

iii

Contents

Preparation of this document iii

Acknowledgements vi

What is epizootic ulcerative syndrome (EUS)? 1

What does epizootic ulcerative syndrome (EUS) do to the fish? 4

History of epizootic ulcerative syndrome (EUS) in Africa 7

Location of the first recorded occurrence in Africa 8

How does epizootic ulcerative syndrome (EUS) occur? 9

How is epizootic ulcerative syndrome (EUS) diagnosed? 10

Which species are susceptible or affected? 12

Which species are not susceptible or affected by epizootic ulcerative syndrome (EUS)? 17

How is epizootic ulcerative syndrome (EUS) spread? What factors cause the fish to become infected with EUS? 18

Why and where is epizootic ulcerative syndrome (EUS) a problem today? 21

Is it safe to eat epizootic ulcerative syndrome (EUS) fish? 24

Can epizootic ulcerative syndrome (EUS)-affected fish be treated? 25

Can infection be prevented? 26

What can one do in the event of a disease outbreak? 28

Can I collect epizootic ulcerative syndrome (EUS) samples for laboratory examination? 29

References 30

Glossary 31

v Acknowledgements

he FAO Fisheries Division (NFI) of the Food and Agriculture Organization of Tthe United Nations (FAO), the FAO project GCP/GLO/979/NOR: “Improving Biosecurity Governance and Legal Framework for Efficient and Sustainable Aquaculture Production” funded by the Norwegian Agency for Development Cooperation and UTF/ZAM/077/ZAM: Technical Assistance to the Zambia Aquaculture Enterprise Development (ZAED): Output 4: Improving Aquatic Animal Health funded by the African Development Bank, and FAO’s Strategic Programme 5, are gratefully acknowledged for support in the preparation and compilation of this publication.

Translation, printing and distribution costs were shouldered by the Southern African Development Community under the leadership of Dr Motseki Hlatshwayo. We also appreciate Prof Kishio Hatai, Dr Gilson Njunga, Dr Ben Van der Waal for providing photos.

vi What is epizootic ulcerative syndrome (EUS)?

pizootic ulcerative syndrome or EUS is the name given to a disease caused Eby an infection with the oomycete fungus known as Aphanomyces invadans or A. piscicida.

Aphanomyces is a member of a group of organisms commonly known as water a moulds; they are currently recognized asb belonging, with diatoms and brown algae, to the group of Stramenopiles (OIE, 2019).This group of organisms contains a number of pathogens of plants and animals that have had devastating effects on agriculture and aquaculture throughout the world. In contrast to free-living saprophytic water moulds, Aphanomyces invadans is an obligate pathogen.

EUS is an epizootic condition affecting wild and farmed freshwater and estuarine finfish since it was first reported in 1971. In affected areas, the disease often occurs seasonally and may be worse in some years.

EUS is also known by other names such as red spot disease (RSD), mycotic granulomatosis (MG), ulcerative mycosis (UM) and in 2005 it was suggested to rename EUS as epizootic granulomatous aphanomycosis (EGA) (Baldock et al. 2005). However the name EUS is most frequently used to describe the disease.

©FAO/B. Van Van der Waal, Namibia ©FAO/B. Figure 1. Enteromius paludinosus – Straightfin barb showing typical epizootic ulcerative syndrome (EUS) lesion. Caprivi Region, Namibia, 2007.

1 AQUAPONICS ©FAO/D. Huchzermeyer, Rhodes University Huchzermeyer, ©FAO/D. Figure 2. Invading hyphae of Aphanomyces invadans (short arrows) with development of typical mycotic granulomas (long arrows) in a histological section of muscle from of an epizootic ulcerative syndrome (EUS)-affected fish (Serranochromis robustus), north Zambia, 2014 (Grocott’s methenamine stain, x40 magnification). ©FAO/D. Huchzermeyer, Rhodes University Huchzermeyer, ©FAO/D. Figure 3. Epizootic ulcerative syndrome (EUS)-affected fish amongst small species (kasepa) harvested by fishermen and laid out onto drying racks in the sun, Bangweulu swamps, north Zambia, 2014.

2 PLATE 7 56 HistopathologyResults of EUS-infected dashtail barb, Barbus poechii (Steindachner, 21 1911), collected by scoop net on 22 May 2007 in the shallow waters of Chobe-Zambezi River in Kasane, Botswana PLATE 7 PLATE 7 56 Histopathology of EUS-infected dashtail barb, Barbus poechii (Steindachner, Histopathology of EUS-infected dashtailPLATEPLATE barb,7 7 Barbus poechii (Steindachner, 1911), collected by scoop net on 22 PLATEMay 2007 7 in the shallow waters of Chobe-Zambezi 1911), collected by scoop net on 22 May 2007 in the shallow waters of Chobe-Zambezi HistopathologyHistopathologyHistopathology of of EUS-infectedof EUS EUS-infected-infectedRiver dashtail in dashtail dashtail Kasane, barb, Barbus barb, barb,Botswana poechii Barbus Barbus (Steindachner, poechii poechii (Steindachner, (Steindachner, 1911), River in Kasane, Botswana 1911), 1911),collected collected collected by byscoopnet by scoop scoop on net net 22 on Mayon 22 22 2007 May May in 2007 2007 the shallowin in the the shallow shallowwaters ofwaters waters Chobe-Zambezi of of Chobe-Zambezi Chobe-Zambezi 20 International Emergency Fish DiseaseRiver Investigation in Kasane, Task Botswana Force Report RiverRiver in in Kasane, Kasane, Botswana Botswana (All photos courtesy of AAHRI)

20 International Emergency Fish Disease Investigation Task Force Report PLATE 6 Histopathology of EUS-infected Thamalakane barb, BarbusBarbus thamalakanensisthamalakanensis,, collected by scoopnet on 22 May 2007 in the shallow waters of Chobe-Zambezi River in Kasane, Botswana (All(All photosphotos PLATEcourtesycourtesy 6 ofof AAHRI)AAHRI) Histopathology of EUS-infected Thamalakane barb, BarbusBarbus thamalakanensisthamalakanensis,, collected by scoopnet on 22 May 2007 in the shallow waters of Chobe-Zambezi River in KPLATEasane, 1Botswana Histopathology of epizootic ulcerative(All(All photosphotos courtesysyndromecourtesy ofof AAHRI)AAHRI) (EUS)-affected Thamalakane barb, EnteromiusHistopathology thamalakanensis of EUS, collected-infected by scoopnet dashtail on barb 22 May Histopathology2007 in the shallow of EUS-infected dashtail barb showing waterstypic of Chobe-Zambezial mycotic Rivergranulomas in Kasane, Botswana showing typical mycotic granulomas surroundingHistopathology the invasive of fungalEUS-infected hyphae dashtail (white barb surrounding Histopathology the of invasiveEUS-infected fungal dashtail hyphae barb Histopathology of EUS-infectedA dashtail barb Histopathology ofB EUS-infected dashtail barb arrows) showinginHistopathologyHistopathology the skin layertypic of ofEUS-infectedal (H&E) EUSmycotic-infected dashtail dashtail barbgranulomas barb(stained HistopathologyHistopathologyshowing black, of typicalbl EUS-infectedofack EUS arrows)-mycoticinfected dashtail in dashtailbarbthegranulomas skin barb layer showingHistopathology typical of EUSmycotic-infected granulomasdashtail barb showingHistopathology typical of EUSmycotic-infected dashtailgranulomas barb surroundingshowingshowing typical typicthe mycotic invasiveal granulomasmycotic fungal surroundinghyphaegranulomas (white showingshowingsurrounding typical typical mycoticthe granulomasinvasivemycotic surrounding fungalgranulomas hyphae showing typical mycotic granulomas (Grocott’ssurroundingshowing silver typicalthe stain)invasive mycotic fungal granulomas hyphae surroundingarrows)surroundingthe invasive in the thefungal invasivethe skin invasive hyphae layer fungal (white (H&E)fungal hyphae arrows) hyphae (whitein the (white thesurrounding(stained invasive black,fungal the hyphaebl ackinvasive (stainedarrows) black, fungalin th blacke skinhyphae layer surroundingskin layer (H&E) the invasive fungal hyphae (white surroundingarrows) in the skinthe layer invasive (Grocott’s silverfungal stain) hyphae arrows)arrows) in the in skinthe skin layer layer (H&E) (H&E) (stained(stained(Grocott’s black, black, silver bl ablck astain)ck arrows) arrows) in in th the eskin skin layer layer arrows) in the skin layer (H&E) (Grocott’s(stained black, silver blstain)ack arrows) in the skin layer (Grocott’s(Grocott’s silver silver stain) stain)

A B PLATE 7 Results 21 Histopathology©FAO/AAHRI of EUS-infected dashtail barb, Barbus poechii (Steindachner,©FAO/AAHRI

1911), collectedA by scoop net on 22 May 2007B in the shallow waters of Chobe-Zambezi C D River in Kasane, Botswana PLATE 7 PLATE 7 Histopathology of EUS-infected dashtail barb, Barbus poechii (Steindachner, Histopathology of EUS-infected dashtailPLATEPLATE barb,7 7 Barbus poechii (Steindachner, 1911), collected by scoop net on 22 PLATEMay 2007 7 in the shallow waters of Chobe-Zambezi 1911), collected by scoop net on 22 May 2007 in the shallow waters of Chobe-Zambezi HistopathologyHistopathologyHistopathology of of EUS-infectedof EUS EUS-infected-infectedRiver dashtail in dashtail dashtail Kasane, barb, Barbus barb, barb,Botswana poechii Barbus Barbus (Steindachner, poechii poechii (Steindachner, (Steindachner, 1911), River in Kasane, Botswana 1911), 1911),collected collected collected by byscoopnet by scoop scoop on net net 22 on Mayon 22 22 2007 May May in 2007 2007 the shallowin in the the shallow shallowwaters ofwaters waters Chobe-Zambezi of of Chobe-Zambezi Chobe-Zambezi River in Kasane, Botswana RiverRiver in in Kasane, Kasane, Botswana Botswana (All photos courtesy of AAHRI) Histopathology of EUS-infected dashtail barb HistopathologyHistopathologyHistopathology of EUS of ofEUS-infected- infectedEUS-infected dashtaildashtail dashtail barb barb barb HistopathologyHistopathology of EUS-infected of EUS- infecteddashtail barb dashtail ba rb

©FAO/AAHRI ©FAO/AAHRI showing typical mycotic granulomas surrounding showingHistopathologyshowingHistopathology typicaltypical mycotic of of EUS EUSgranulomas-infectedmycotic-infected surrounding dashtail dashtailgranulomas ba barbrb showingHistopathologyshowing Histopathologytypical typicalof EUSofmycotic EUS-infectedmycotic-infected granulomasdashtail dashtailgranulomas barb barb Histopathologyshowing typical of EUS -infectedmycotic dashtailgranulomas barb C Histopathologyinvasive fungal hyphaeof EUS (white-infected Darrows) dashtail penetrating barb invasiveshowing fungal hyphaetypical (stained mycotic black, blackgranulomas arrows) Typical mycoticshowing granulomasshowing (indicatedtypical typical by black mycotic arrow)mycotic found granulomas in thegranulomas muscle tissue surroundingshowing showing ofsurrounding fish sample typical typicalinvasiveNo. 1 invasive mycoticmycotic fungalfungal hyphaehyphaegranulomasgranulomas (stained(stained Enteromiussurrounding thamalakanensisshowingsurroundinginto theinvasive (Thamalakane muscletypical invasive layer fungal (H&E)barb).mycotic fungal (A)hyphae muscle hyphae tissuesgranulomas (white with(white mycotic penetrating surroundinggranulomas into(H&E); invasivethe muscle fungallayer (Grocott’s hyphae silver (stained surrounding invasive fungal hyphae (whiteblack,surrounding surroundingblack, black black invasive invasivearrows) arrows) fungalfungal penetratingpenetrating hyphaehyphae (stained(stainedinto the the Typical(B) oomycete mycoticarrows) hyphae surroundinggranulomassurrounding arrows)penetrating penetrated (indicated penetratinginvasive into invasive bythe intoblack brain fungal arrow) ofthefungalinto the foundfish; musclehyphaethe hyphae(B), in musclethe (C) muscle and(white layer(white (D) tissuelayer are stainedof stain) fishblack, samplewith blackGrocott’s No. 1 Barbus stain.arrows) penetrating into the thamalakanensisthamalakanensis (Thamalakane(Thamalakanearrows) barb).barb).penetrating (A)(A) musclemuscle tissuestissuesinto withwiththe mycoticmycoticmuscle granulomasgranulomas layermuscleblack, (H&E);(H&E);black,muscle (B)(B) layerblack oomyceteoomyceteblack layer (Grocott’s arrows) (Grocott’sarrows) penetrating silverpenetrating silver stain). stain). intointo thethe (H&E).arrows)arrows) (H&E). penetrating penetrating into into the the muscle muscle layerlayer muscle layer (Grocott’s silver stain). hyphae penetrated into(H&E). the brain of the fish; (B), (C) and (D) are stained with Grocott’smusclemuscle stain layer layer (Grocott’s (Grocott’s silver silver stain). stain). C (H&E).(H&E). D PLATE 2

TypicalHistopathology mycotic granulomas of epizootic (indicated ulcerative by black arrow) found in the muscle tissue of fish sample No. 1 Barbus thamalakanensissyndromethamalakanensis (EUS)-affected (Thamalakane(Thamalakane barb).barb).dashtail (A)(A) musclemusclebarb, tissuestissues withwith mycoticmycotic granulomasgranulomas (H&E);(H&E); (B)(B) oomyceteoomycete HistopathologyhyphaeEnteromius penetrated of EUS poechii -intoinfected. Chobethe brain dashtail River of the infish; Kasane,barb (B), (C) Histopathologyand (D) are stained withof Grocott’sEUS-infected stain dashtail barb showing Botswana,typical 2007. mycotic granulomas showing typical mycotic granulomas

surroundingHistopathology the invasive of fungalEUS-infected hyphae dashtail (white barb surrounding Histopathology the of invasiveEUS-infected fungal dashtail hyphae barb Histopathology of EUS-infected dashtail barb Histopathologyshowing typicalof EUS -infectedmycotic dashtail granulomas barb arrows) showinginHistopathologyHistopathology the skin layertypic of ofEUS-infectedal (H&E) EUSmycotic-infected dashtail dashtail barbgranulomas barb(stained HistopathologyHistopathology black, of bl EUS-infectedofack EUS arrows)-infected dashtail in dashtailbarbthe skin barb layer ©FAO/AAHRI Histopathology of EUS-Dashtailinfected dashtail barb, Barbus barb showingHistopathology poechii (Steindachner,typical of EUSmycotic-infected 1911), dashtail exhibitinggranulomas barb haemorrhagic dermatitis showingsurroundingshowing typicaltypic theal mycotic invasivemycotic granulomasDashtail fungal granulomas surrounding hyphaebarb, Barbus (white poechiishowingshowingsurrounding typical (Steindachner, typical mycoticthe granulomasinvasivemycotic 1911), surrounding fungalexhibitinggranulomas hyphae haemorrhagic dermatitis showingshowing typictypicalal Dashtail Dashtailmycoticmycotic barb, barb,granulomas granulomasBarbus Barbus pospoechii Dashtail(Grocott’s poechiishowingDashtailterior (Steindachner,barb, to (Steindachner,barb, anussilver Barbus typicalEnteromius and stain) poechii towards 1911), poechii,mycotic 1911), (Steindachner, the exhibitingexhibiting exhibiting caudalgranulomas 1911), peduncle. haemorrhagic haemorrhagic dermatitis dermatitis surroundingthe invasive the fungal invasiveDashtail hyphae fungal (whitebarb, hyphae arrows) Barbus (whitein the poechii possurroundingteriorthe (Steindachner,invasive to anus fungalthe and hyphaeinvasive towards 1911), (stained thefungal black,exhibiting caudal blackhyphae peduncle. haemorrhagic dermatitis arrows)surrounding in the the skin invasive layer (H&E)fungal hyphae (whiteexhibiting surroundinghaemorrhagicsurrounding(stained haemorrhagic black, dermatitisthethe bl ainvasiveckinvasive dermatitis posterior arrows) fungalto fungalposteriorin anus th eand skinhyphaehyphae to layer arrows)surroundingskin inlayer the (H&E) skinthe invasivelayer (H&E) fungal hyphaepos (whiteposteriorposterior (stainedterior arrows)to to anus to anus black,inanus the and and skin andbl towards atowardslayerck towards arrows) (Grocott’s the the in silvercaudalcaudal caudalthe stain) skin peduncle. peduncle. layer arrows) in the skin layer (H&E) anustowards(stained(Grocott’s and towardsthe black, caudal silver the bl peduncle. astain)caudalck arrows) peduncle in the skin layer arrows) in the skin layer (H&E) (Grocott’s(stained black, silver blstain)ack arrows) in the skin layer (Grocott’s(Grocott’s silver silver stain) stain)

©FAO/AAHRI ©FAO/AAHRI HistopathologyHistopathology of of EUS EUS-infected-infected dashtail babarb rb HistopathologyHistopathologyHistopathology of EUS of of ofEUS-infected -epizootic infectedEUS-infected ulcerative dashtaildashtail dashtail barb syndrome barb barb Histopathology of of EUS-infected epizootic ulcerative dashtail barb syndrome showing typical mycotic granulomas surrounding showingHistopathologyshowingHistopathologyshowing typical typical mycotic typicalof of EUS EUSgranulomas -infectedmycotic-mycoticinfected surrounding dashtail dashtailgranulomas ba barbrb showingHistopathologyHistopathologyshowing Histopathology(EUS)-affectedtypical typicalof of EUSdashtailofmycotic EUS EUS-infected- mycoticinfectedbarb-infected showing granulomasdashtail dashtail dashtailgranulomas typical barb barb barb Histopathology(EUS)-affected dashtailof EUS barb-infected showing dashtail typical barb showinginvasive fungal typical hyphae (whitemycotic arrows) penetratinggranulomas surroundingshowing invasiveshowingsurrounding fungal typical invasivehyphaetypical invasive (stained mycotic fungalmycoticfungal black, hyphaeblackhyphaegranulomasgranulomas arrows) (stained(stained surroundingshowingshowingsurroundingintomycotic theinvasive muscle typicalgranulomastypical invasive layer fungal (H&E) mycoticsurroundingmycotic fungal hyphae hyphaegranulomasinvasivegranulomas (white fungal(white showingpenetratingmycotic granulomas intotypical the muscle surrounding mycotic layer (Grocott’s invasive granulomas silver fungal surrounding invasive fungal hyphae (whitesurrounding surrounding invasive invasive fungal fungal hyphae hyphae (stained(stained arrows)surroundingsurrounding arrows)hyphaepenetrating (white penetratinginvasive invasive arrow)into fungal penetratingthefungalinto musclehyphaethe hyphae intomuscle the(white layer(white muscle layer black, surroundingstain)hyphaeblack, black(stained black invasive black,arrows) arrows) black fungal penetratingarrow)penetrating hyphae penetrating (stainedinto the the arrows) penetrating into the muscle layerblack, black, black black arrows) arrows) penetratingpenetrating intointo thethe arrows)arrows)(H&E).layer penetrating(H&E). penetrating into into the the muscle muscle layerlayer muscleblack,intomuscle the layer muscleblack layer (Grocott’s layer (Grocott’sarrows) (Grocott´s silverpenetrating silver silver stain). stain). stain). into the (H&E). (H&E). musclemuscle layer layer (Grocott’s (Grocott’s silver silver stain). stain). (H&E).(H&E). muscle layer (Grocott’s silver stain). 3

DashtailDashtail barb, Barbus poechii (Steindachner,(Steindachner, 1911), 1911), exhibiting exhibiting haemorrhagic haemorrhagic dermatitis dermatitis Dashtail barb, BarbusDashtail poechii barb, (Steindachner, Barbus poechii 1911), (Steindachner, exhibiting 1911), haemorrhagic dermatitis DashtailDashtail barb, barb, Barbus Barbus poechii pospoechiiteriorterior (Steindachner, (Steindachner, toto anusanus andand towards towards 1911),1911), the the exhibitingexhibiting caudal caudal peduncle. peduncle. haemorrhagic haemorrhagic dermatitis dermatitis posposteriorexhibitingterior to to anus haemorrhagicanus and and towards towards dermatitis the the caudal caudalposterior peduncle. peduncle. to posterioranus to and anus towards and thetowards caudal pedunclethe caudal peduncle.

What does epizootic ulcerative syndrome (EUS) do to the fish? Clinical signs of EUS in affected fish showing the range of lesions

US causes unsightly lesions in affected fish. EUS-affected fish may swim Eslowly, show abnormal swimming movements, and in rivers may be observed near the riverbanks swimming with the current where healthy fish swim against the current. Sick fish will also seek out shallow vegetated areas of still waters. ©FAO/D. Huchzermeyer, Rhodes University Huchzermeyer, ©FAO/D. Figure 5. Labeo lunatus – upper Zambezi labeo with early lesion of epizootic ulcerative syndrome (EUS). Note red appearance of the lesions and swelling of the surrounding tissue, Chobe River, Botswana, 2007 (Andrew et al., 2008). ©FAO/D. Huchzermeyer, Rhodes University Huchzermeyer, ©FAO/D. Figure 6. Clarias gariepinus – Sharptooth catfish affected by epizootic ulcerative syndrome (EUS) showing both the red spots that are typical of early infection and the large, deep ulcers that develop later. Fish sampled during an EUS outbreak, Bangweulu swamps, north Zambia, 2014.

4 Lesions can range from small pinpoint red spots, haemorrhagic spots, localized swelling and localized raised areas on the body surface with protruding scales or scale loss to skin erosion, exposure of underlying musculature and extensive ulceration.

Ulcers or ‘wounds’ can be found over a broad area of the body with the center of the lesions containing dead tissue.

Lesions are observed most often on the lateral surface but can also occur on any part of the body. ©FAO/R. Bills, South African Institute of Aquatic Biodiversity Aquatic of African Institute Bills, South ©FAO/R. Figure 7. Enteromius poechii – Dashtail barb with typical early lesion of epizootic ulcerative syndrome (EUS), Kabompo River, upper Zambezi, 2010 (Huchzermeyer and Van der Waal, 2012). ©FAO/D. Huchzermeyer, Rhodes University Huchzermeyer, ©FAO/D. Figure 8. Marcusenius macrolepidotus – Northern bulldog. Note the unilateral ulcerating lesion typical of epizootic ulcerative syndrome (EUS) at the base of the pectoral fin, Equateur Province, Democratic Republic of Congo (DRC), 2015.

5 ©FAO/O. Weyl South African Institute of Aquatic Aquatic of African Institute South Weyl ©FAO/O. Biodiversity Figure 9. Hydrocynus vittatus – Tigerfish. Extensive dermal ulceration typical of epizootic ulcerative syndrome (EUS), Okavango River, 2010 (Huchzermeyer and Van der Waal, 2012). ©FAO/B. Van Van der Waal, Namibia ©FAO/B. Figure 10. Brycinus lateralis - silver robber with early lesions typical of epizootic ulcerative syndrome (EUS) possibly associated with preceding predator injury to the skin, Kafue River, Zambia, 2007. ©FAO/B. Van Van der Waal, Namibia ©FAO/B. Figure 11. Serranochromis macrocephalus - purpleface largemouth with an advanced lesion typical of epizootic ulcerative syndrome (EUS) showing extensive ulceration, fish farm, Caprivi, Namibia, 2008. ©FAO/D. Huchzermeyer, Rhodes University Huchzermeyer, ©FAO/D. Figure 12. Parachanna obscura – Snakehead. Note ulcerating lesions typical of epizootic ulcerative syndrome (EUS) in the tail region of a fish sampled, Equateur Province, Democratic Republic of Congo (DRC), 2015. 6 History of epizootic ulcerative syndrome (EUS) in Africa

ollowing on reports of large numbers of fish with ulcers in the Chobe River Fon the border between Botswana and Namibia in 2006 (Figure 13), surveys initiated in February 2007 revealed the condition to be present in fish in the Chobe River in the vicinity of the Chobe Game Reserve in Botswana, the Caprivi Region of Namibia and on the Zambian side of the Zambezi River above Victoria Falls. The disease was subsequently confirmed as the first outbreak of EUS on the African continent. In this area, EUS-infected fish have been observed seasonally at the end of subsequent summers, but with a lower prevalence. Reports from Zambia have indicated a rapid spread upstream in the Zambezi River and some of its tributaries, in some cases associated with large-scale fish mortality, as well as in the Kafue River. In 2010, outbreaks of EUS in fish were reported from the Okavango Delta in Botswana, and in 2011, from Lake Liambezi in Namibia. Three outbreaks of EUS were reported from Western Cape Province of South Africa in 2011 and 2012. The disease was first noticed affecting a number of fish species in an artificial impoundment on the Palmiet River, and in a farm dam on the Eerste River. A further outbreak in the Limpopo catchment in the North West Province of South Africa was reported in 2014.

Other cases were reported from estuarine fish in the Western Cape Province in 2015, and in 2016 from a river in the Western Cape Province and from an impoundment in the Northern Cape Province. A single case was reported from the Kruger National Park in Limpopo Province in 2017. The first occurrence of EUS in the headwaters of the Congo River was reported from the Bangweulu Wetlands in the north of Zambia in 2014, where in subsequent years, the disease reappeared annually at the end of the rainy season. The first outbreak of EUS in the Democratic Republic of Congo, affecting the Equateur Province in the north west of that country, was confirmed and reported in 2015. Zimbabwe reported two outbreaks of EUS for the first time in 2016 from Mashonaland East and Midlands Provinces with further outbreaks reported subsequently. Reports of EUS from Malawi were made for the first time in July 2020 from the Bua River in the Central Province. Following no reports of disease from Botswana since 2010, an outbreak of EUS associated with high mortality was again reported from the Chobe River in July 2020.

In Southern Africa, EUS has had its greatest impact on floodplains, and flood plain fisheries have been particularly hard hit. The annual flooding cycle in the floodplains of the Zambezi system and elsewhere creates conditions particularly favourable to outbreaks of EUS.

7 Location of the first recorded occurrence in Africa

Map conforms to United Nations Map No. 4170 Rev. 18.1 UNITED NATIONS February 2020.

Figure 13. First recorded occurrence of epizootic ulcerative syndrome (EUS) in the Chobe River on the border between Botswana and Namibia, 2006.

©FAO/C. Huchzermeyer, Bangweulu Wetlands, African Parks Wetlands, Bangweulu Huchzermeyer, ©FAO/C. Figure 14. Climbing perch, Ctenopoma multispine, a species frequently affected by epizootic ulcerative syndrome (EUS) during the annual outbreaks of epizootic ulcerative syndrome (EUS) that have occurred in the Bangweulu swamps, north Zambia, since 2014 (Huchzermeyer et al., 2018).

8 How does epizootic ulcerative syndrome (EUS) occur?

easonal climatic conditions can create Senvironments that favour occurrence of EUS. In many parts of Africa, for instance, the drop in temperature at the end of the rainy season, seasonal draining of floodplains during the winter months and flood-drought cycles that favour acidification of surface waters have been associated with outbreaks of EUS.

Infection in fish leading to EUS occurs when motile spores (zoospores) of A. invadans are released into the water from infected fish or other carriers/vectors. The zoospores are attracted to the skin of the fish.

The spores penetrate compromised areas of skin and germinate, forming fungal filaments or hyphae.

The hyphae invade widely into the surrounding skin and deeply into the underlying muscle, resulting in extensive destruction of tissues leading to ulceration.

The hyphae will produce sporangia that eventually release further motile spores. 402/2 Paper Technical Fisheries Hatai and FAO ©FAO/K. The sporangia are narrow, with diameters Figure 15. Typical characteristic of similar to that of the hyphae. Aphanomyces sporangium (Japanese isolate). A single row of primary zoospores formed within a zoosporangium are then released through the sporangium to encyst at the apical tip of the sporangium to form achlyoid clusters. From here, the main free- swimming stage of Aphanomyces spp., the secondary zoospore, is discharged into the water to seek out a further fish to infect.

©S. Kanchanakhan (June 2007) (June Kanchanakhan ©S. Figure 16. Sporulation of the Botswana oomycete isolate successfully identified as Aphanomyces by the Aquatic Animal Health Research Institute (AAHRI), Thailand, June 2007.

9 How is epizootic ulcerative syndrome (EUS) diagnosed? ©FAO/D. Huchzermeyer, Rhodes University Huchzermeyer, ©FAO/D. Figure 17. Serranochromis robustus – Nembwe. Note the deep ulcer containing white necrotic tissue in a fish affected by epizootic ulcerative syndrome (EUS), Luwombwa River, north Zambia, during 2014.

ften the first indication of EUS is the presence of ulcerative skin lesions that Oare commonly found in freshwater and estuarine fishes in infected waters.

The presence of lesions often indicates a contaminated or stressed aquatic environment and may be associated with a variety of infections including parasites, bacteria, viruses and fungi, as well as non-infectious causes such as for example toxic algae. Intra-species aggression is believed to be a predisposing factor in some species such as snakehead fish.

Presumptive diagnosis of EUS can be based on Level 1 diagnosis consisting of observation of gross appearance (red spots and open dermal ulcers) and Level II diagnosis using a microscope to detect aseptate branching hyphae in squashed preparations of the muscle underlying gross lesions.

Confirmatory diagnosis requires: 1. histological demonstration of the typical granulomatous inflammation around invasive hyphae (Level II diagnosis) or, 2. isolation of Aphanomyces invadans from the underlying muscle (Level III diagnosis) or, 3. demonstration of genetic material belonging to A. invadans by molecular laboratory means (Level III diagnosis).

10 ©FAO/D. Huchzermeyer, Rhodes University Huchzermeyer, ©FAO/D. Rhodes University Huchzermeyer, ©FAO/D. Figure 18. Appearance of hyphae of Figure 19. Appearance of hyphae of Aphanomyces invadans within sheaths of Aphanomyces invadans in a histological macrophages within an area of necrotic section of muscle stained with Grocott’s muscle in a histological section stained methenamine stain (x400 magnification). with haematoxylin and eosin (x400 Note that the walls of the hyphae stain magnification). The sample was collected almost black and are surrounded by a sheath from a Labeo lunatus suffering from epizootic of macrophages (arrows) within necrotic ulcerative syndrome (EUS), Botswana, muscle tissue. The sample was collected from 2007 outbreak period. Long arrows point to Labeo lunatus during the 2007 outbreak of hyphae in longitudinal section, short arrows epizootic ulcerative syndrome (EUS), Chobe point to hyphae in cross section. River, Botswana. ©FAO/R. Bills, South African Institute of Aquatic Aquatic of African Institute Bills, South ©FAO/R. Biodiversity Figure 20. Hepsetus odoe – African pike. Note the ulcerative lesion typical of epizootic ulcerative syndrome (EUS) near the anal fin, Kabompo River, upper Zambezi, 2010.

Figure 21. Enteromius paludinosus with epizootic ulcerative syndrome (EUS) lesions, Kasungu Water Board

©G. Njunga reservoir dam, Malawi, 2020.

11 Which species are susceptible or affected?

ore than 160 species, worldwide, are susceptible to EUS, including farmed, Mwild, freshwater and estuarine fish. Many of these have been reported from the Zambezi floodplains. ©FAO/D. Huchzermeyer, Rhodes University Huchzermeyer, ©FAO/D. Figure 22. Clarias gariepinus – Sharptooth catfish with multiple deep ulcers caused by infection with Aphanomyces invadans, from the Bangweulu swamps, north Zambia, 2014. ©FAO/R. Peel, Department of Ichthyology and fisheries Science, Rhodes University Department of Ichthyology Peel, ©FAO/R. Figure 23. Serranochromis robustus – Nembwe with a deep ulceration typical of epizootic ulcerative syndrome (EUS), below Popa Falls, Okavango River, Nambia, July 2010 (Huchzermeyer and Van der Waal, 2012).

12 Table 1. Fish species from which infection with Aphanomyces invadans has been reported in Southern and Central Africa (updated from FAO, 2009)

Sources: Scientific name Common name Country with confirmed diagnosis (year) Brycinus lateralis Striped robber Namibia (2007) – FAO (2009) Caprivi, Zambezi (2007)* Caffrogobius nudiceps Barehead goby South Africa (2015) Clarias sp. Catfish Zambia (2007) – FAO (2009) Caprivi, Zambezi (2007)* Clarias gariepinus Sharptooth catfish Namibia (2007) – FAO (2009) Zambia (2008) – FAO (2009) Caprivi, Zambezi (2007)* South Africa (2011) Zimbabwe (2018) Botswana (2020) Clarias ngamensis Blunttooth catfish Namibia (2007) – FAO (2009) Zambia (2007) – FAO (2009) Caprivi, Zambezi (2007)* Zimbabwe (2018) Botswana (2020) Clarias theodorae Snake catfish Democratic Republic of Congo (2015) – FAO (2017) Coptodon rendalli Redbreast tilapia Namibia (2008) – FAO (2009) Caprivi, Zambezi (2007)*, Zimbabwe (2016) Botswana (2020) Ctenopoma multispine Climbing perch Zambia (2014) Enteromius haasianus Sickle-fin barb Namibia (2014) Enteromius paludinosus Straightfin barb Namibia (2007) – FAO (2009) Caprivi, Zambezi (2007)*, Zambia (2014), Zimbabwe (2016) Zimbabwe (2018) Enteromius poechii Dashtail barb Botswana (2007) – FAO (2009) Namibia (2007) – FAO (2009) Zambia (2007) – FAO (2009) Caprivi, Zambezi (2007)* Zimbabwe (2018) Enteromius thamalakanensis Thamalakane barb Botswana (2007) – FAO (2009) Enteromius trimaculatus Threespot barb Zambia (2014) Enteromius unitaeniatus Longbeard barb/slender barb Namibia (2008) – FAO (2009) Caprivi, Zambezi (2007)* Namibia (2014) Hepsetus odoe African pike Namibia (2007) – FAO (2009) Zambia (2007) – FAO (2009) Caprivi, Zambezi (2007)* Botswana (2010) Hydrocynus vittatus Tigerfish Namibia (2007) – FAO (2009) Caprivi, Zambezi (2007)* Labeo capensis Orange River mudfish South Africa (2016) Labeo cylindricus Redeye labeo Namibia (2008) – FAO (2009) Caprivi, Zambezi (2007)* Labeo lunatus Upper Zambezi labeo Botswana (2007) – FAO (2009) Namibia (2007) – FAO (2009) Caprivi, Zambezi (2007)* Lepomis macrochirus Bluegill sunfish South Africa (2011) Marcusenius macrolepidotus Northern bulldog Namibia (2007) – FAO (2009) Caprivi, Zambesi (2007)* Micralestes acutidens Sharptooth tetra/silver robber Namibia (2007) – FAO (2009) Caprivi, Zambezi (2007)*

13 Table 1. (Continued)

Sources: Scientific name Common name Country with confirmed diagnosis (year) Micropterus salmoides Largemouth bass South Africa (2011) Zimbabwe (2018) Micropterus dolomieu Smallmouth bass South Africa (2016) Mormyrus lacerda Western bottlenose Onchorhynchus mykiss Rainbow trout South Africa (2011) Oreochromis andersonii Threespot tilapia Namibia (2007) – FAO (2009) Zambia (2007) – FAO (2009) Caprivi, Zambezi (2007)* Zimbabwe (2018) Oreochromis macrochir Greenhead tilapia Namibia (2007) – FAO (2009) Caprivi, Zambezi (2007)* Oreochromis mossambicus Mozambique tilapia Zimbabwe (2016) Oreochromis shiranus Shire tilapia Malawi (2020) Parachana obscura Snakehead Democratic Republic of Congo (2015) – FAO (2017) Petrocephalus catostoma Northern Churchill Botswana (2008) – FAO (2009) Caprivi, Zambezi (2007)* Democratic Republic of Congo (2015) – FAO (2017) Pharyngochromis acuticeps Zambezi happy/Zambezi river Namibia (2008), suspected – FAO (2009) bream Caprivi, Zambezi (2007)*, Zambia (2007-2008) Pollimyrus isidori Elephantfish Zambia (2014) Protopterus annectens Lungfish Democratic Republic of Congo (2015) – (2017) Sargochromis carlottae Rainbow bream/happy Namibia (2008) – FAO (2009) Sargochromis codringtonii Green bream Namibia (2008) – FAO (2009) Zambia (2007) – FAO (2009) Caprivi, Zambezi (2007)* Sargochromis giardi Pink bream Namibia (2008) – FAO (2009) Caprivi, Zambezi (2007)* Schilbe intermedius Silver catfish/butter barbel Namibia (2007) – FAO (2009) Zambia (2007) – FAO (2009) Caprivi, Zambezi (2007)* Botswana (2010) Serranochromis angusticeps Thinface largemouth Namibia (2008), suspected – FAO (2009) Zambia (2007) – FAO (2009) Caprivi, Zambezi (2007)* Serranochromis macrocephalus Purpleface largemouth Namibia (2008), suspected – FAO (2009) Caprivi, Zambezi (2007)* Serranochromis robustus Nembwe/Tsungwa Namibia (2007), suspected – FAO (2009) Zambia (2007) – FAO (2009) Caprivi, Zambezi (2007)* Zimbabwe (2018) Synodontis sp. Squeaker Democratic Republic of Congo (2015) – FAO (2017) Botswana (2020) Tilapia ruweti Okavango tilapia Tilapia sparmanii Banded tilapia Namibia (2008) – FAO (2009) Caprivi, Zambezi (2007)* Botswana (2020) * Caprivi, Zambezi (2007) from Huchzermeyer and Van der Waal (2012).

14 ©G. Njunga Figure 24. Clarias gariepinus, Enteromius paludinosus and Petrocephalus catostoma with multiple lesions of epizootic ulcerative syndrome (EUS), Bua River, Mchinji District, Malawi, July 2020. ©FAO/D. Huchzermeyer, Rhodes University Huchzermeyer, ©FAO/D. Figure 25. Parachanna obscura – Snakehead. Note deeply ulcerating lesions associated with epizootic ulcerative syndrome (EUS) extending into the bony structures of the head, Equateur Province, Democratic Republic of Congo (DRC), 2015. ©FAO/D. Huchzermeyer, Rhodes University Huchzermeyer, ©FAO/D. Figure 26. Enteromius paludinosus – Straightfin barb with an early lesion typical of epizootic ulcerative syndrome (EUS), Bangweulu swamps, north Zambia, 2014.

15 ©FAO/C. Huchzermeyer, Bangweulu Wetlands, African Parks Wetlands, Bangweulu Huchzermeyer, ©FAO/C. Figure 27. Clarias gariepinus – Sharptooth catfish. Note the deeply ulcerative lesion exposing underlying dead muscle tissue typical of epizootic ulcerative syndrome (EUS), Bangweulu swamps, north Zambia, 2014.

Figure 28. Clarias gariepinus with lesions of epizootic ulcerative syndrome (EUS), Lusa River, Mchinji District,

©G. Njunga Malawi, July 2020.

Figure 29. Clarias gariepinus with lesions of epizootic ulcerative syndrome (EUS), Lusa River, Mchinji District, Malawi, July 2020. ©G. Njunga

16 Which species are not susceptible or affected by EUS?

ile tilapia (Oreochromis niloticus), common carp (Cyprinus carpio) and milk Nfish Chanos( chanos) are believed to be naturally resistant to infection with Aphanomyces invadans.

Nile tilapia and common carp are frequently farmed species in Africa and feral populations are widespread in some natural waters. ©FAO/D. Huchzermeyer, Rhodes University Huchzermeyer, ©FAO/D. Figure 30. Oreochromis niloticus – Nile tilapia. Farmed fish such as this one from a farm on Lake Kariba, Zimbabwe, have been extensively introduced for aquaculture in Zambia and Zimbabwe. ©FAO/T. Sinclair, Lydenburg, South Africa South Lydenburg, Sinclair, ©FAO/T. Figure 31. Cyprinus carpio – Common carp. An introduced species that has become feral in some freshwater systems in Southern and Central Africa and is popular with recreational fishermen.

17 How is epizootic ulcerative syndrome (EUS) spread? What factors cause the fish to become infected with EUS?

uccessful invasion and establishment of EUS in fish requires epithelial tissue Sdamage, a susceptible fish species and environmental conditions which favour sporulation of A. invadans.

In some countries, outbreaks occur in wild fish first and then spread into fish ponds.

A number of risk factors are associated with EUS occurrence; some are predisposing factors, others are environmental conditions and biological factors that contribute to the occurrence of EUS.

Shipping movements, ballast water, fish migrations and ocean currents are potential pathways by which the pathogen can spread between water bodies.

Cross border movement of fish for aquaculture and the ornamental fish trade are proven pathways by which the disease spreads.

Some EUS outbreaks follow heavy rainfall and flood events; reductions in water temperature, alkalinity and salinity; and acidified run-off water from acid sulphate soil areas have been associated with outbreaks of disease.

Parasites and rhabdoviruses have also been associated with particular outbreaks, and secondary gram-negative bacteria invariably infect EUS lesions. ©FAO/D. Huchzermeyer, Rhodes University Huchzermeyer, ©FAO/D. Figure 32. Fishing nets may be infected with spores of Aphanomyces invadans and should be dried immediately after use, and not be left where they remain wet as in this picture, Bangweulu swamps, north Zambia, 2014 outbreak of epizootic ulcerative syndrome (EUS).

18 ©FAO/D. Huchzermeyer, Rhodes University Huchzermeyer, ©FAO/D. Figure 33. The ornamental variety of the common carp (koi) is a popular and often valuable fish that is imported into many countries for ornamental purposes. Some varieties of koi have been shown to be susceptible to epizootic ulcerative syndrome (EUS). ©D. K. Hatai ©D. K. Hatai ©D. ©D. K. Hatai ©D. FigureGold 34. fish, Gold Carassius fish, Carassius carassius auratus auratus, is a popular is the and susceptibility widely traded to ornamental Aphanomyces fish that is Goldknown fish,piscicida to Carassius be susceptible. (Hatai, 1980)tocarassius epizootic ulcerative auratus syndrome is the (EUS). susceptibility to Aphanomyces Goldpiscicida fish, Carassius. (Hatai, carassius 1980) auratus is the susceptibility to Aphanomyces piscicida. (Hatai, 1980)

19 ©FAO/D. K. Hatai ©FAO/D. K. Hatai ©FAO/D. Figure 35. Aphanomyces invadans infection in dwarf gourami, another popular ornamental fish species susceptible to epizootic ulcerative syndrome (EUS), (K. Hatai et al., 1994). AphanomycesAphanomyces invadans invadans infection infection in dwarf in dwarf gourami gourami (Hatai (Hatai et al., et 1994)al., 1994) ©FAO/D. K. Hatai ©FAO/D. K. Hatai ©FAO/D. ©FAO/D. K. Hatai ©FAO/D. K. Hatai ©FAO/D. Figure 36. Hyphae in muscle squash preprations of lesions of ayu Plecoglossus altivelis with mycotic granulomatosis (Arrow: granuloma).

20 Why and where is epizootic ulcerative syndrome (EUS) a problem today? EUS is one of the most serious aquatic diseases known to affect finfish. The disease causes high losses to fish farmers and fishermen through mortalities and reduced productivity of all susceptible fish species. Market rejection and public health concerns due to the presence of unsightly lesions provide for further losses.

EUS has been reported from at least 28 countries and from four continents (North America, Africa, Asia and Australia).

More than 160 species of finfish are susceptible to EUS. Almost a third of these occur in Southern and Central Africa.

Other indirect long-term effects include the threat to the environment and aquatic biodiversity through, for example, declining fish numbers and irreversible ecological damage.

EUS has the potential to financially decimate those who rely on fishing for income. In addition, and perhaps more importantly, EUS outbreaks threaten food security for subsistence fishers and fish farmers and consequently people’s physical health, as fish forms an important source of animal protein for people in many affected countries.

The spread of EUS across Asia from Japan and Australia where it was first identified in the early 1970s to Pakistan in 1996 and to southern Africa in 2006 is a major epizootiological phenomenon.

EUS is an OIE-listed disease, and notification to the World Organization for Animal Health (or OIE) is required in the event of an outbreak.

21 Map showing the current global Figure 37. Chronology of global occurrence of distribution of epizootic ulcerative EUS; dates with question mark indicate outbreaks of ulcerative fish disease and/or unconfirmed EUS syndrome (1971 to 2020) outbreaks; dates without question mark indicate year of EUS confirmation (Lilley et al., 1998; Baldock et al., 2005; FAO, 2009). Japan (1971); Australia (Queensland – 1972, New South Wales – 1989, Northern Territory – 1990 and Western Australia – 1994); Papua New Guinea (1975 –1976?; 1982–1983?; 1986); Indonesia (1980?; 1993–1994); Singapore (1977?); Malaysia (1979?; 1980); Thailand (1981); Myanmar, Lao People’s Democratic Republic and

150 120 90 60 30 0 30 60 90 120 150 180

1 BOSNIA AND HERZEGOVINA THE WORLD 2 CROATIA 3 SERBIA Greenland 4 MONTENEGRO (Denmark) 5 SLOVENIA 6 NORTH MACEDONIA

Alaska (U.S.A.) ICELAND SWEDEN FINLAND NORWAY RUSSIAN FEDERATION 60 60 ESTONIA UNITED LATVIA DENMARK KINGDOM R.F. LITHUANIA CANADA NETHERLANDS IRELAND POLAND BELARUS BELGIUM GERMANY UKRAINE LUXEMBOURG CZECHIA SLOVAKIA FRANCE AUSTRIA KAZAKHSTAN HUNGARY REP. OF MOLDOVA St. Pierre SWITZERLAND 5 2 MONGOLIA LIECHTENSTEIN ROMANIA and Miquelon (Fr.) ANDORRA 1 3 SAN BULGARIA UZBEKISTAN DEM. PEOPLE'S MARINO ITALY 4 GEORGIA MONACO 6 KYRGYZSTAN REP. OF KOREA SPAIN HOLY SEE ALBANIA ARMENIA AZERBAIJAN PORTUGAL TURKEY GREECE TURKMENISTAN TAJIKISTAN UNITED STATES OF AMERICA SYRIAN Jammu and REPUBLIC JAPAN TUNISIA CYPRUS ARAB REP. MALTA ISLAMIC Kashmir * OF KOREA Bermuda (U.K.) LEBANON REP.OF AFGHANISTAN CHINA ISRAEL IRAQ MOROCCO IRAN 30 JORDAN 30 PAKISTAN ALGERIA KUWAIT NEPAL BHUTAN LIBYA BAHRAIN BAHAMAS EGYPT Western QATAR UNITED ARAB Sahara SAUDI EMIRATES INDIA MEXICO Turks and Caicos Islands (U.K.) BANGLADESH ARABIA LAO PEOPLE'S CUBA DEM. REP. Hawaii DOMINICAN REPUBLIC OMAN MYANMAR Northern (U.S.A.) HAITI CABO VERDE MAURITANIA BELIZE JAMAICA Mariana Puerto Rico (U.S.A.) ANTIGUA AND BARBUDA MALI NIGER ST. KITTS AND NEVIS Islands (U.S.A.) GUATEMALA HONDURAS ST. VINCENT AND THE GRENADINES SENEGAL SUDAN ERITREA YEMEN THAILAND PHILIPPINES DOMINICA BURKINA CHAD VIET NAM EL SALVADOR NICARAGUA ST. LUCIA BARBADOS GAMBIA Guam (U.S.A.) GRENADA FASO GUINEA-BISSAU DJIBOUTI CAMBODIA TRINIDAD AND TOBAGO GUINEA BENIN COSTA RICA PANAMA MARSHALL VENEZUELA SIERRA LEONE GHANA NIGERIA SOUTH ETHIOPIA SRI LANKA ISLANDS GUYANA CENTRAL BRUNEI PALAU SURINAME CÔTE SUDAN LIBERIA CAMEROON AFRICAN REP. DARUSSALAM French Guiana (Fr.) D'IVOIRE TOGO COLOMBIA SOMALIA MALDIVES MALAYSIA FEDERATED STATES OF MICRONESIA EQUATORIAL GUINEA UGANDA SINGAPORE 0 CONGO KENYA 0 SAO TOME AND PRINCIPE GABON KIRIBATI ECUADOR DEMOCRATIC RWANDA NAURU Tokelau (N.Z.) REPUBLIC OF BURUNDI THE CONGO INDONESIA TUVALU ANGOLA UNITED REP. Chagos PAPUA (Cabinda) OF TANZANIA Archipelago (Mauri.) NEW GUINEA SOLOMON Marquesas (Fr.) Ascencion (U.K.) SEYCHELLES Wallis and Christmas TIMOR LESTE ISLANDS COMOROS Agaleda Island (Austr.) Futune Islands PERU (Fr.) BRAZIL ANGOLA MALAWI Cocos (Keeling) SAMOA ZAMBIA Tromelin Island Islands (Austr.) American Cargados Carajos Shoals VANUATU FIJI Samoa (U.S.A.) French BOLIVIA St. Helena (U.K.) Society MOZAMBIQUE Niue (N.Z.) Polynesia Gambier Is. (Fr.) ZIMBABWE Rodriges Island Arch. MADAGASCAR (Fr.) NAMIBIA (Fr.) MAURITIUS TONGA Cook BOTSWANA Réunion New Caledonia Islands PARAGUAY (Fr.) (Fr.) (N.Z.) Pitcairn AUSTRALIA Austral Is. Islands ESWATINI (U.K.) (Fr.) 30 SOUTH 30 AFRICA LESOTHO The boundaries and names shown and the designations used CHILE URUGUAY on this map do not imply official endorsement or acceptance by the United Nations. ARGENTINA Tristan da Cunha (U. K.) Final boundary between the Republic of Sudan and the Republic of South Sudan has not yet been determined. Gough (U.K.) *Dotted line represents approximately the Line of Control NEW in Jammu and Kashmir agreed upon by India and Pakistan. ZEALAND The final status of Jammu and Kashmir has not yet been agreed upon by the parties.

**A dispute exists between the Governments of Argentina and Falkland Islands (Malvinas) (U.K.)** the United Kingdom of Great Britain and Northern Ireland concerning sovereignty over the Falkland Islands (Malvinas). South Georgia (U.K.) The initials in parentheses refer to the administering Power or the Power involved in a special treaty relationship.

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ANTARCTICA Map No. 4170 Rev. 18.1 UNITED NATIONS Office of Information and Communications Technology February 2020 Geospatial Information Section 150 120 90 60 30 0 30 60 90 120 150 180

22 Cambodia (1983 or 1984); Viet Nam (1983?); China (1982?; 1987–1988?; 1989?); China, Hong Kong SAR (1988?); Philippines (1985); Sri Lanka (1987); Bangladesh (1988); India (1988); Bhutan and Nepal (1989); Pakistan (1996); United States of America (North Carolina, Florida and Connecticut – 1984); Botswana (2006?; 2007; 2010; 2020); Namibia (2006?; 2007); Zambia (2007?; 2008; 2014); Canada (2010); Zimbabwe (2016); South Africa (2011; 2014; 2015; 2016; 2017); Democratic Republic of Congo (2015); Malawi (2020).

150 120 90 60 30 0 30 60 90 120 150 180

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ANTARCTICA Map No. 4170 Rev. 18.1 UNITED NATIONS Office of Information and Communications Technology February 2020 Geospatial Information Section 150 120 90 60 30 0 30 60 90 120 150 180 Map produced by N.H. Huchzermeyer, Rhodes University, using ArcMapTM 10.6 software. Map conforms to United Nations Map No. 4170 Rev. 18.1 UNITED NATIONS February 2020. 23 Is it safe to eat epizootic ulcerative syndrome (EUS) fish? The agent causing EUS does not pose any direct human health risk. The deep ulcerations and tissue decay in fish infected with EUS may harbour secondary pathogens which may have health implications to humans consuming such fish.

Thorough cooking may destroy pathogens, such as A. invadans. However, fish tissues compromised by EUS may spoil rapidly and render a product of inferior nutritional value. It is therefore advisable to avoid eating fish showing gross lesions of EUS. ©FAO/D. Huchzermeyer, Rhodes University Huchzermeyer, ©FAO/D. Figure 38. It is believed that traditional methods such as smoking used to preserve fish products, as in the case of these fish in the Democratic Republic of Congo (DRC) in 2015, will destroy the agent of epizootic ulcerative syndrome (EUS).

24 Can epizootic ulcerative syndrome (EUS)-affected fish be treated?

here is no known treatment by which EUS-affected fish can be treated. TControl of EUS in natural waters (e.g. rivers) is impossible.

Fish farmers whose farmed fish have been affected with EUS are encouraged to culture, where possible, non-EUS susceptible species or avoid farming susceptible species during the season when EUS is prevalent, i.e. high rainfall period and low temperature season.

A strict ban on the movement of fish from infected waterways or river systems, especially those with lesions of EUS, to other waterways or river systems is recommended; diseased fish should not be moved from one fish farm to another.

Particular care should be taken when moving resistant species, such as Nile tilapia, from hatcheries situated on potentially infected waters. Fish species susceptible to EUS may inhabit the water source of a hatchery and shed infectious spores of Aphanomyces invadans into the water. These can be readily transferred with transport water in which fry and fingerlings are sold.

Properly dried, salted and iced fish have not been reported as potential carriers of EUS, therefore trade of these products can be allowed to continue. ©FAO/D. Huchzermeyer, Rhodes University Huchzermeyer, ©FAO/D. Figure 39. Clarias gariepinus – African sharptooth catfish showing early and advanced lesions of epizootic ulcerative syndrome (EUS), Bangweulu swamps, north Zambia, 2014.

25 Can infection be prevented?

number of important biosecurity measures can minimize or prevent the Aspread of EUS. These include: ➔ All possible carriers or vectors such as freshly dead fish, birds or terrestrial animals as well as contaminated fishing gears/nets and fish transport containers should be prevented from getting into water bodies or fish ponds. ➔ In outbreaks occurring in small, closed water bodies, disinfection of destocked ponds by liming and improvement of water quality, together with removal of infected fish, are often effective in reducing mortality. ➔ Increasing salinity in holding waters to above 2 parts per thousand may also prevent outbreaks of EUS in aquaculture ponds. ➔ During dry and cold seasons, close observation of wild fish should be made to determine the presence of EUS–diseased fish in neighbouring tanks or canals, in which case, exchange of water should be avoided. ➔ EUS infected fish should never be thrown back into open waters and should be disposed of properly by burying them into the ground or through incineration (burning). ©FAO/D. Huchzermeyer, Rhodes University Huchzermeyer, ©FAO/D. Figure 40. Fish that have died as a result of epizootic ulcerative syndrome (EUS), such as this Clarias gariepinus, should be removed from the water. As the fish decays large numbers of Aphanomyces invadans spores can be released into the water, Bangweulu swamps, north Zambia, 2014.

26 ➔ Additional practical aquaculture biosecurity measures should be implemented, including: – improved farm hygiene (e.g. handwashing between tanks, separation of nets/tanks/stocks, regular and correct disinfection procedures, etc.) – optimal husbandry practices – optimal water quality management – proper handling of fish – regular monitoring of fish health – good record keeping (gross and environmental observations and stocking records including movement records of fish in and out of the aquaculture facility, etc.) ➔ Early reporting or notification to concerned authorities of a disease outbreak or suspicion of any abnormal appearance, behaviour or other observations in fish stocks.

27 What can one do in the event of a disease outbreak?

➔ Immediately stop all live fish movements (quarantine). ➔ Dry and disinfect all fishing gear and boats before moving to another water body. ➔ Report immediately a suspected outbreak to concerned authorities (nearest fisheries or veterinary authority) and ask for guidance concerning collection of samples (see page 29). ➔ The abnormal congregation of aquatic birds feeding on fish has been typical of some outbreaks of EUS observed in Botswana and Zambia and may draw attention to presence of large numbers of sick fish. ➔ Taking note of simple observations that deviate from the normal will assist in Level I diagnosis and surveillance and will help to alert to presence of EUS. Abnormal swimming behavior such as swimming near the surface, swimming with the current, sinking to the bottom, loss of balance, flashing and cork-screw swimming and in non-airbreathing fish gulping at the surface are all indications of sick fish. If any of these observations are noted together with presence of red spots and ulcers/wounds on the fish this will be a strong indication of EUS. ➔ It is important to note the date and time of observed disease outbreaks to determine annual patterns during which fishermen and aquaculturists should be alert for the dangers of EUS. ➔ Further important information to record is the species of fish affected, an estimate of mortality (numbers of fish found dead) and the pattern of mortality (small number of fish dying each day, large number of fish dying at one time, etc.). ➔ Adverse climatic events such as flooding following on drought, sudden cold spells and the presence of disturbed soils that might cause acid leaching into waters should be recorded. ➔ Anticipation of outbreaks and early warning allow containment measures to be instituted timeously. These may include the need for additional disinfection of fishing equipment, discouraging fishermen from moving between EUS- affected and non-affected waters with their fishing gear, avoiding sourcing water for fish farms from water ways that might be contaminated with the zoospores of Aphanomyces invadans during an outbreak of EUS and avoiding moving fingerlings for fish farming from hatcheries on EUS-affected water sources. During an EUS outbreak, a ban on trade in fish across provincial and national borders and between catchments may be instituted by the authorities to reduce the spread of EUS.

28 Can I collect epizootic ulcerative syndrome (EUS) samples for laboratory examination?

➔ Live samples, if available, are best for laboratory examination. The fish should be packed in double plastic bags, filled with water to one third of their capacity with the remaining 2/3 volume inflated with air/oxygen. Bags should be tightly sealed (with rubber band or tape) and protected from temperature fluctuation. ➔ If live fish that can be transported to the laboratory are not available, freshly dead or moribund/sick fish with clinical lesions can be used. ➔ Using a scalpel or a blade, take samples of skin/muscle sections (<1 cm3), including the edge of the lesion and the surrounding tissue. Parts of internal organs may also be collected by dissecting the whole fish. ➔ Fix the tissue samples immediately in 10 percent formalin (10 ml of formalin in 90 ml of water, preferably phosphate-buffered saline made up in distilled water) in a plastic or bottled container. The amount of formalin should be 10 times the volume of the tissue to be fixed. Tissues should be fixed for at least 24 hours before processing. ➔ After 24 hours, fixed tissues can be wrapped into formalin-moistened tissue paper and placed into small plastic bags to prevent leakage or smell during transport. ➔ Using a scalpel or a blade, collect a second smaller sample of muscle (<0.5 cm3) from the edge of the lesion. ➔ Fix the muscle tissue immediately in 90-100 percent ethanol. ➔ Make sure that samples are properly labelled with the following information: date of sampling, type of tissue samples (e.g. skin, muscle, gills, kidney, other internal organs), collection locality (place of collection), species of fish (weight and length measurements if possible), name of collector, type of fixative used (10 percent formalin, etc.). ©FAO/D. Huchzermeyer, Rhodes University Huchzermeyer, ©FAO/D. ➔ Samples can be packed Figure 41. Positions relative to a typical epizootic into a padded envelope or ulcerative syndrome (EUS) lesion in Clarias gariepinus container and sent by mail from which suitable samples can be dissected for fixation if no courier services exist. in (a) 10% formalin - sample should include skin and ➔ Call the laboratory to inform muscle and extend from the ulcer into surrounding of the kind of samples healthy appearing tissue, and (b) 90-100% ethanol - the skin is removed and the underlying muscle is sampled collected and when they adjacent to the edge of the ulcer or below the ulcer), are expected to arrive or to Bangweulu swamps, north Zambia, 2014. be delivered.

29 References

Andrew, T.G., Huchzermeyer, K.D.A., Mbeha, B.C. & Nengu, S.M. 2008. Epizootic ulcerative syndrome affecting fish in the Zambezi River system in southern Africa,Veterinary Record 163: 629–632. (also available at http://dx.doi.org/10.1136/vr.163.21.629,PMid:19029110). Baldock, F.C., Blazer, V., Callinan, R., Hatai, K., Karunasagar, I. Mohan, C.V. & Bondad-Reantaso, M.G. 2005. Outcomes of a short expert consultation on epizootic ulcerative syndrome (EUS): re-examination of causal factors, case definition and nomenclature.In P. Walker, R. Lester and M.G. Bondad-Reantaso (eds). Diseases in Asian Aquaculture V, pp. 555–585. Fish Health Section, Asian Fisheries Society, Manila. Blazer, V., Bondad-Reantaso, M.G., Callinan, R.B., Chinabut, S., Hatai, K., Lilley, J.H. & Mohan, C.V. 2005. Aphanomyces invadans (A. piscicida): A Serious Pathogen of Estuarine and Freshwater Fishes, pp. 24–41. In Cipriano, R.C., Shchelkunov, I.S. and Faisal, M. (editors). Health and Diseases of Aquatic Organisms: Bilateral Perspectives. Proceedings of the Second Bilateral Conference Between Russia and the United States. 21–18 September 2003. Sheperdstown, West Virginia. Michigan State University, East Lansing, Michigan. Bondad-Reantaso, M.G., McGladdery, S., East, I. & Subasinghe, R.P. (eds). 2001. Asia diagnostic guide to aquatic animal diseases. FAO Fisheries Technical Paper No. 402. Supplement 2. Rome, FAO. 240p. Choongo, K., Hang’ombe, B., Samui, K.L., Syachaba, M., Phiri, H. & Maguswi, C. 2009. Environmental and climatic factors associated with epizootic ulcerative syndrome (EUS) in fish from the Zambezi floodplains, Zambia.Bulletin of Environmental Contamination and Toxicology, 83: 474–478. (also available at http://dx.doi.org/10.1007/s00128-009-9799-0, PMid:19565173). FAO. 2009. Report of the international emergency disease investigation task force on a serious fish disease in Southern Africa, 18-26 May 2007. Rome, Italy. (also available at http://www.fao.org/ docrep/012/i0778e00.htm). FAO. 2017. Report of the International Emergency Fish Disease Investigation Mission on a Suspected Outbreak of Epizootic Ulcerative Syndrome (EUS) in the Democratic Republic of the Congo, 13–19 March 2015. Rome, Italy. (also available at http://www.fao.org/3/a-i6596e.pdf). Hatai, K., Nakamura, K., An Rha, S., Yuasa, K. & Wada, S. 1994. Aphanomyces infection in dwarf gourami (Colisa lalia). Fish Pathology., 29, 95–99 Huchzermeyer, K.D.A. & Van der Waal, B.C.W. 2012. Epizootic ulcerative syndrome: Exotic fish disease threatens Africa’s aquatic ecosystems.Journal of the South African Veterinary Association 83(1), Art. #204, 6 pages. (also available at http://dx.doi.org/10.4102/jsava.v83i1.204). Huchzermeyer, C.F., Huchzermeyer, K.D.A., Christison, K.W, Macey, B.M, Colly, P.A., Hangombe, B.M. & Songe M.M. 2 01 7. First-record of epizootic ulcerative syndrome from the Upper Congo catchment: an outbreak in the Bangweulu swamps, Zambia. Journal of Fish Diseases. 41(1): 87-94, DOI:10.1111/jfd.12680 Kaphuka, B., Njunga, G. R., Kamwendo, G. & Chirwa, B. B. 2020. Active surveillance of infection caused by Aphanomyces invadans in Malawi. International Journal of Fisheries and Aquaculture (12) 1-5 (also available at http://doi: 10.5897/IJFA2019.0728). Lilley, J.H., Callinan, R.B., Chinabut, S., Kanchanakhan, S., MacRae, I.H. & Phillips, M.J. 1998. EUS Technical Handbook. AAHRI, Bangkok. 88pp. OIE. 2019. Manual of Diagnostic Tests for Aquatic Animals. World Organization for Animal Health, Paris. Malherbe, W., Christison, K.W., Wepener, V. & Smit, N.J. 2019. Epizootic ulcerative syndrome – First report of evidence from South Africa’s largest and premier conservation area, the Kruger National Park IJP: Parasites and Wildlife (10) 207-210 (also available at https://doi.org/10.1016/j. ijppaw.2019.08.007) McHugh, K.J., Christison, K.W., Weyl, O.L.F. & Smit, N.J. 2014. Histological confirmation of epizootic ulcerative syndrome in two cyprinid species from Lake Liambezi, Zambezi Region, Namibia. African Zoology 49(2), 311–316. Nsonga, A., Mfitilodze, W., Samui, K.L. & Sikawa, D. 2012. Epidemiology of epizootic ulcerative syndrome in the Zambezi River system. A case study for Zambia.Human and Veterinary Medicine. International Journal of the Bioflux Society, 5(1):1-8. Sibanda, S., Pfukenyi, D. M., Barson, M., Hang’ombe, B. & Matope, G. 2018. Emergence of infection with Aphanomyces invadans in fish in some main aquatic ecosystems in Zimbabwe: A threat to national fisheries production.Transboundary and Emerging Diseases: 1–9.DOI: 10.1111/ tbed.12922 Songe, M.M., Hang’ombe, M.B., Phiri, H., Mwase, M., Choongo, K., Van der Waal, B., Kanchanakhan, S., Reantaso, M. B. & Subasinghe, R. P. 2012. Field observations of fish species susceptible to epizootic ulcerative syndrome in the Zambezi River basin in Sesheke District of Zambia. Tropical Animal Health and Production, 44:179–183 DOI 10.1007/s11250-011-9906-1

30 Glossary

Disease Any deviation from or interruption of the normal structure or function of any part, organ, or system (or combination thereof) of the body that is manifested by a characteristic set of symptoms and signs and whose aetiology, pathology and prognosis may be known or unknown. Epidemiology Science concerned with the study of the factors determining and influencing the frequency and distribution of disease or other health related events and their causes in a defined population for the purpose of establishing programmes to prevent and control their development and spread. Epizootic Affecting many animals at the same time; widely diffused and rapidly spreading disease (syn. Epidemic – used for human disease). Epizootiology The study of factors influencing infection by a pathogenic agent. Fungi Heterotrophic organisms possessing a chitinous* wall, with the majority of fungal species growing as multicellular filaments called hyphae forming a mycelium. Fungi are more closely related to animals than plants, yet the discipline of biology dedicated to the study of fungi, known as mycology, often falls under a branch of botany. * Note that in contrast to the true fungi, the oomycetes, of which Aphanomyces is a member, have a cellulose cell wall.

Granulomas Any small nodular delimited aggregation of inflammatory cells, or modified macrophages resembling epithelial cells (epithelioid cells) formed by the body to ward off an infection or foreign substance. Granulomatosis Any condition characterized by the formation of multiple granulomas. Heterokonts Or stramenopiles are a major line of eukaryotes presently containing about 10 500 known species; includes the group oomycetes to which Aphanomyces invadans belongs. As opposed to higher fungi, the oomycetes have a cell wall composed of cellulose. Infection Invasion and multiplication of an infectious organism within host tissues. May be clinically benign (cf subclinical or carrier) or result in cell or tissue damage. The infection may remain localized, subclinical and temporary if the host defensive mechanisms are effective or it may spread to form an acute, sub- acute or chronic clinical infection (disease). Lesion Any pathological or traumatic change in tissue form or function. Mycology The study of fungi (Mycota). Mycosis Any disease resulting from infection by a fungus.

31 Glossary

Oomycetes A group of filamentous, unicellular heterokonts or stramenopiles physically resembling fungi; they are microscopic, absorptive organisms that reproduce both sexually and asexually and are composed of mycelia. The genus Aphanomyces is known to produce only by asexual means. Outbreak The sudden onset of disease in epizootic proportions. Pathogen An infectious agent capable of causing disease. Predispose To make susceptible to a disease that may be activated by certain conditions, as by stress. Sporangium (Mycology) hyphal swelling which contains motile or non-motile zoospores; release is via a pore or breakdown of the sporangial wall (syn. zoosporangium). Spore Infective stage of an organism that is usually protected from the environment by one or more protective membranes (syn. zoospores). Sporogenesis Formation of or reproduction by spores; sporulation. Stress The sum of biological reactions to any adverse stimuli (physical, internal or external) that disturb the organism’s optimum operating status. Susceptible An organism which has no immunity or resistance to infection by another organism. Syndrome An assembly of clinical signs which when manifest together are indicative of a distinct disease or abnormality (syn. pathognomic/ pathognomonic). Ulcer Excavation of the surface of an organ or tissue, involving sloughing of necrotic inflammatory tissue.

32 ©FAO/D. Huchzermeyer, Rhodes University Huchzermeyer, ©FAO/D. Rhodes University Huchzermeyer, ©FAO/D. Figure 42. Use of a sturdy scoop net is ideal for sampling Figure 43. Typical catch of small fish species in a gill net small sick fish from the shallows along a river’s edge left over night during surveillance for epizootic ulcerative during an epizootic ulcerative syndrome (EUS) outbreak, syndrome (EUS)-affected fish, Chobe River, Botswana, Chobe River, Botswana, 2007. 2007.

©FAO/D. Huchzermeyer, Rhodes University Huchzermeyer, ©FAO/D. Rhodes University Huchzermeyer, ©FAO/D. Figure 44. Shallow vegetated areas of wetlands often Figure 45. Bemba speaking fishermen with a seasonal harbour sick fish during an epizootic ulcerative syndrome catch of small flood plain fish being preserved by drying (EUS) outbreak. Scoop nets are ideal for sampling such in the sun (traded as kasepa). During epizootic ulcerative areas, Bangweulu swamps, north Zambia, 2014. syndrome (EUS) outbreaks, infected fish can readily be observed on drying racks, Bangweulu swamps, north Zambia, 2014.

33 ©FAO/D. Huchzermeyer, Rhodes University Huchzermeyer, ©FAO/D. Rhodes University Huchzermeyer, ©FAO/D. Figure 46. Inspecting live air-breathing fish for signs of Figure 47. Fishermen searching for epizootic ulcerative epizootic ulcerative syndrome (EUS) at a fish market, syndrome (EUS)-affected fish from a pirogue during Equateur Province, Democratic Republic of Congo an EUS investigation, Equateur Province, Democratic (DRC), 2015. Republic of Congo (DRC), 2015.

©FAO/D. Huchzermeyer, Rhodes University Huchzermeyer, ©FAO/D. Rhodes University Huchzermeyer, ©FAO/D. Figure 48. Searching for fish showing signs of epizootic Figure 49. Rivers draining tropical rain forests in Africa ulcerative syndrome (EUS) in the shallows along a river often have a low pH of 4.5 favouring outbreaks of bank. Note the red-brown colour of the water associated epizootic ulcerative syndrome (EUS), Equateur Province, with low pH typical of waters draining from tropical rain Democratic Republic of Congo (DRC), 2015. forests, Equateur Province, Democratic Republic of Congo (DRC), 2015.

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