Invasive Zoopathogenic Mastigomycotina in Republika Srpska, Serbia and Neighboring Countries with Special Reference to Aphanomyces Astaci

Зборник Матице српске за природне науке / Jour. Nat. Sci, Matica Srpska Novi Sad, № 124, 341—354, 2013

UDC 582.28:616.993(497.6+497.11) DOI: 10.2298/ZMSPN1324341V

Slobodanka B. Vujčić1, Svjetlana B. Lolić2, Mara M. Bojić3, Predrag B. Ilić4, 5 5 Milana S. Novaković , Maja A. Karaman , Milan N. Matavulj5

1 University of Business Studies, Banja Luka, Republika Srpska 2 Faculty of Sciences, Department of Biology, University of Banja Luka, Republika Srpska 3 Fond for Environmental Protection of Republika Srpska, Banja Luka, Republika Srpska 4 Institute of Environmental Protection, Ecology and Informatics, Banja Luka, Republika Srpska 5 Department of Biology and Ecology, Faculty of Natural Sciences, University of Novi Sad, Republic of Serbia

INVASIVE ZOOPATHOGENIC MASTIGOMYCOTINA IN REPUBLIKA SRPSKA, SERBIA AND NEIGHBORING COUNTRIES WITH SPECIAL REFERENCE TO APHANOMYCES ASTACI

ABSTRACT: Non-native alien zoopathogens have had a profound impact on the health of aquatic zoobiota in Republika Srpska and the Republic of Serbia as well as around the region and the world as a whole. The movement of disease-causing microfungi around the world has taken its toll on many different organisms, and continues to intensify with an increase in global transport of cargo, people, and animals. Those who study fungi have little information about the characteristics of invasive, zopathogenic fungi because of the fact that a particular fungus can inhabit many different organisms, and may be pathogenic to some of these hosts but not to the others. Crayfish plague (Aphanomyces astaci) broke out through the Danube River to the territory of Bačka and Banat (today A.P. Vojvodina, the Republic of Serbia) in 1879. Until 1880, the disease spread through the Sava River to the northern Bosnia (today Republika Srpska). From 1955 until 1970, almost all territories of Republika Srpska and Republic of Serbia were afflicted with the crayfish plague disease. Despite the fact that the problems of the spread of crayfish plague in the territory of the Republika Srpska and the Republic of Serbia have been of great significance, there is little data available for analyzing this issue. According to IUCN criteria, and mostly due to the Aphanomyces astaci invasion, the degree of endangerment of noble crayfish in Serbia was evaluated as “Endangered”, which was a higher degree than the international level determined for this species, i.e., “Vulnerable”. KEY WORDS: fungi, invasive, Aphanomyces astaci, Republika Srpska, the Repub- lic of Serbia

341 INTRODUCTION

The commonly used definition of biological invasions, in scientific communities, implies negative ecological impact. The term ‘invasive’ covers any non-indigenous species that has spread and become abundant in a new geographical location regardless of the actual ecological impact (P e t i t et al., 2004; D e s p r e z-L o u s t a u et al., 2007). By using this definition, it can be concluded that fungi with economic, but unknown ecological impact, should be regarded as invaders (Tab. 1). Successful invaders can be defined as species able to pass through a series of filters corresponding to the successive steps of the invasion: transport, establishment and spread (K o l a r and L o d g e, 2001; R i c h a r d s o n et al., 2000; S a k a i et al., 2001). Unlike plant and animal invasions, deliberate introductions have probably had a minor role in fungal introductions. Desirable fungi that were introduced in new habitats mostly included pathogenic fungi used for classical biological control (CBC). Few examples of fungal invasions, resulting from the escape of purposefully introduced pathogenic fungi, were reported (S e l o s s e et al., 1998).

Tab. 1. – Potential or reported ecological interactions among zoopathogenic Mastigomycotina

Interaction Result Examples References Crayfish plague Aphanomyces Specialist pathogen astaci (Saprolegniaceae, (relatively) in natural Oomycota) (Europe), carried D a s z a k et al., 2000; Emerging ecosystem; host–patho- by introduced North American A l d e r m a n, 1996, disease gen not coevolved crayfish, with chronic infections, (host jump) transmitted to native European crayfish Frog chytrid Batrachochytrium D a s z a k et al., 2000; Generalist pathogen dendrobatidis (Chytridiomycota, B r i g g s et al., 2010; in natural ecosystem; Emerging Chytridiomycetes, Rhizophydi- R a c h o w i c z et al., host–pathogen not disease ales) (North America and 2005; F i s h e r et al., coevolved (host jump) Europe) 2009; M o r e l, 1999 Vectors of Saprolegnia ferax, a pathogen exotic and of amphibians, is greater in native toad population exposed to Animals that interact parasites; hatchery-reared trout; Exotic R i z z o, 2005; with native and inva- increase in reptiles can serve as vectors of W e b b e r, 1990 sive fungal parasites population Basidiobolus ranarum (causes of native basidiobolomycosis in humans, parasites horses and other vertebrates)

With the exception of a few well known examples of invasive animal pathogens, microfungi are generally poorly represented in date bases of invasive or alien species. Emerging infectious diseases can be defined as diseases caused by pathogens showing new or increased geographical range, new host range or caused by new or recently evolved pathogens. Fungi is the important

342 Tab. 2. – Fungi in available databases of invasive species (D e s p r e z-L o u s t a u et al., 2007)

Region List Fungi Source Austria Neobiota (invasive) 83 E s s l and R a b i t s c h (2002) England Non-native species 198 H i l l, M. et al. (2005) Latvia Alien species 7 http://lv.invasive.info/ Lithuania Invasive species 98 http://www.ku.lt/lisd/ Nordic–Baltic states Alien species 98 http://sns.dk/nobanis/ Poland Alien species 81 http://www.iop.krakow.pl/ias/ Switzerland Alien species (invasive) 6 Wittenberg R (2005) http://www.issg.org/database/ World Global invasive species (worst) 9 welcome/ taxonomic group, responsible for emerging infectious diseases in general, and introduced pathogens have also been recognized as an important cause of emerging diseases in animals, although fungi are less present among animal pathogens (D a s z a k et al., 2000; D o b s o n and F o u f o p o u l o s, 2001). (Tab. 2). The most obvious impacts of fungal invasions were epidemics (zoonoses) caused by exotic pathogenic fungi. It was estimated that 65–85% of pathogens worldwide were alien at the location where they were recorded (P i m e n t e l et al., 2001). Such invasions can have significant ecological, economic and social consequences. Despite of the fact that these species exist in neighboring countries (Ta- ble 3) or in more remote European countries (Table 4), in Republika Srpska and Bosnia and Herzegovina, just a few species were registered as invasive, such as ascomycete Cryphonectria parasitica (Murrill) Barr., nominated as one of “World’s worst” invaders (http://www.issg.org/database/species/ecology. asp?si=124&fr=1&sts=sss &lang=EN). Even though “fungal” species, belong- ing to Mastigomycotina group, represents a significant cause of serious diseases on various groups of organisms, there are no evidence on this group in any of the databases, neither in Bosnia and Herzegovina, in First national Report for the Convention on Biodiversity, (Federal Ministry of Environment and Tour- ism of Bosnia and Herzegovina, 2008), nor in the Republic of Serbia (Table 4). However, P a v l o v i ć et al. (2006) reported about the first finding of Or- conectes (Faxonius) limosus in the Serbian part of the River Danube, what could lead to the indirect conclusion on the replacement of almost extinct Astacus astacus.

RESULTS OF ANALYSED AVAILABLE DATA

The list of aquatic animal diseases/pathogens and susceptible species that are considered for monitoring purposes with regard to the zoning and ap- proval of an area/farm in Bosnia and Herzegovina listed Aphanomyces astaci, causing the well known disease crayfish plague, with no further comments or explanations (A l a g i ć, 2009).

343 Tab. 3 – Non-indigenous invasive species Aphanomyces astaci (Oomycetes, Mastigomycotina) in Republika Srpska and the Republic of Serbia, in neighboring and regional countries

Recent Country Source finding http://www.cbd.int/invasive/doc/legislation/Greece.pdf Albania http://www.iucnredlist.org/details/2431/0 F r a n k e 1894 Austria A l d e r m a n, 1996 http://www.oie.int/wahis_2/public/wahid.php/Diseaseinformation/ statusdetail Bosnia and http://www.iucnredlist.org/details/153745/0 Herzegovina A l a g i ć 2009 A l d e r m a n, 1996 H u b e n o v a et al. 2010 Bulgaria 2010 A l d e r m a n, 1996 http://www.iucnredlist.org/details/2430/0 P â r v u l e s c u et al. 2012 Croatia 2012 A l d e r m a n, 1996 http://www.iucnredlist.org/details/2191/0 K o z u b í k o v á et al. 2006, 2009 2009 Czech http://www.oie.int/wahis_2/public/wahid.php/Diseaseinformation/ 2011 Republic statusdetail 2012 A l d e r m a n, 1996 T h e o c h a r i s 1986 Greece http://www.cbd.int/invasive/doc/legislation/Greece.pdf K o z u b í k o v á et al. 2010 Hungary 2010 A l d e r m a n, 1996 C o r n a l i a 1860 C a m m à et al. 2010 2009 A q u i l o n i et al. 2011 Italy 2010 http://www.iucnredlist.org/details/2430/0 2011 http://www.oie.int/wahis_2/public/wahid.php/Diseaseinformation/ statusdetail Not reported till 2000 Macedonia http://www.oie.int/wahis_2/public/wahid.php/Diseaseinformation/ FYR statusdetail No available data Montenegro http://www.oie.int/wahis_2/public/wahid.php/Diseaseinformation/ statusdetail P â r v u l e s c u et al. 2012 Romania 2012 S c h r i m p f et al. 2012 A l d e r m a n, 1996 http://www.iucnredlist.org/details/2191/0 Slovakia J a n s k ý and K a u t m a n 2007 A l d e r m a n, 1996 Slovenia A l d e r m a n, 1996 H a r l i o ğ l u 2008 2008 Turkey K o k k o et al. 2012 2012 B a r a n and S o y l u 1989

344 According to the OIE (2012), Aphanomyces astaci is a member of the group of organisms commonly known as the water molds. Although regarded to be fungi for a long time, this group, the Oomycetes, is now considered pro- tists and are classified with diatoms and brown algae in a group called the Stra- menopiles or Chromista. Four groups (A–D) of A. astaci were described based on random amplification of polymorphic DNA polymerase chain reaction (D i e g u e z - U r i b e o n d o et al., 2009): Group A (the so called Astacus strains) comprises a number of strains that were isolated from Astacus astacus and Astacus leptodactylus; these strains are thought to have been in Europe for a long period of time. Group B (Pacifastacus strains I) includes isolates from both A. astacus in Sweden and Pacifastacus leniusculus from Lake Tahoe, the USA. Imported P. leniusculus have probably introduced A. astaci and infected the native A. astacus in Europe. Group C (Pacifastacus strains II) consists of a strain isolated from P. leniusculus from Pitt Lake, Canada. Another strain (Pc), isolated from Procambarus clarkii in Spain, falls into group D (Procambarus strain). This strain shows temperature/growth curves with higher optimum temperatures compared with the isolates from northern Europe (D i e g u e z - U r i b e o n d o et al., 1995). Aphanomyces astaci strains that have been present in Europe for many years (group A strains) appear to be less pathogenic than strains which have been introduced more recently with crayfish imports from North America since the 1960s. The crayfish plague is a well documented example of fungal zoonoses (Table 3, Table 4). The fungus Aphanomyces astaci (Saprolegniaceae, Oomy- cota), which causes the well known disease crayfish plague, was introduced to Italy, probably through ballast water discharge from North American ship in 1860 (C o r n a l i a, 1860). It was also spread to other countries: to Sweden in 1907, Spain in 1958, Norway in 1971, the United Kingdom in 1981, and Turkey in 1987 (D i é g u e z-U r i b e o n d o, 1997; O i d t m a n n et al., 1997). The plague wiped out native populations of the noble European crayfish (Astacus astacus) almost to the point of extinction in some countries. In the Greece’s Actions on IAS report (2010), Aphanomyces astaci was listed as the major invasive alien species, (http://www.cbd.int/invasive/doc/legislation/Greece.pdf), and L o w e et al., (2004) considered this fungus as one of the 100 of the world’s worst invasive alien species. The most comprehensive review on the spread of crayfish plague was presented by A l d e r m a n (1996). Importantly, crayfish plague continued to spread in Europe because American crayfish species continued to spread on the continent by natural movements or due to stocking by humans (e.g. the American signal crayfish and red swamp crayfish). The signal crayfish (Paci- fastacus leniusculus) was introduced as a replacement in waters where Asta- cus astacus had been, or had almost been extinct, what caused new problems since signal crayfish, being immune to the disease and as a carrier of infection, increased the spread of the plague to previously unaffected populations of noble crayfish (H o l d i c h, 1988). Aphanomyces astaci can be transferred from one water body to the next also through fishing gear, contaminated traps, by the transfer of infected animals, and probably even by predators

345 Tab. 4 – Non-indigenous invasive species Aphanomyces astaci (Oomycetes, Mastigomycotina) in Republika Srpska and the Republic of Serbia, and in more remote European countries

Country Source Belarus A l d e r m a n, 1996 N y l u n d and W e s t m a n 1992 Finland W e s t m a n and N y l a n d 1979 France A l d e r m a n, 1996 O i d t ma n n et al. 1997 S c h ä p e r c l a u s 1927 Germany S u r b e c k 1903 A l d e r m a n, 1996 A l d e r m a n, 1996 Ireland R e y n o l d s 1988 M a t t h e w s and R e y n o l d s 1990 Italy http://www.iucnredlist.org/details/2430/0 M a n n sf i e l d 1942 Latvia A l d e r m a n, 1996 T z u k e r z i s 1964 Lithuania M a z y l i s and G r i g e l i s 1979 A l d e r m a n, 1996 V r å l s t a d, et al. 2011 Norway T a u g b ø l et al. 1993 A l d e r m a n, 1996 D i é g u e z-U r i b e o n d o 2006 Spain http://www.oie.int/wahis_2/public/wahid.php/Diseaseinformation/statusdetail A l m 1929 Sweden B o h m a n et al. 2006 A l d e r m a n, 1996 A r n o l d 1900 Russia A l d e r m a n, 1996 H o f e r 1900 Ukraine A l de r m a n, 1996 O i d t m a n n et al. 2005 A l d e r m a n et al. 1984 EUK H o g g e r 1984 http://www.iucnredlist.org/details/2430/0 preying on crayfish (N y l u n d & W e s t m a n 1992, O i d t m a n n et al., 2005). Beside the crayfish plague, most fungal diseases affecting freshwater crayfish are associated with poor water quality which has to be achieved by environmental management. Fungicides or general disinfectants, such as for- malin, may be used for identification of causes of fungal infections. There are no cures for crayfish plague infection. Normally, 100% of susceptible crayfish species in a population will be killed after the fungus is introduced. (http:// www.crayfishmates.com/crayfish_diseases/fungi.html). The recent worldwide outbreaks of amphibian chytridiomycosis, which contributed to the population decline, might also be caused by anthropogenic

346 introduction of the pathogen, Batrachochytrium dendrobatidis, outside its endemic range (R a c h o w i c z et al., 2005).

DISCUSSION

The first pioneering attempt in the Republic of Serbia to make provisional list of invasive fungal species was done within the Project on “Invasive alien species in Vojvodina”, which lasted from 2005 to 2010, and was supported by the Republic Fond for the Environmental Protection, coordinated with the Provincial Secretariat for the Environmental Protection and Techno- logical Development of Autonomous Province of Vojvodina. Seven fungal species were listed in this provisional list and two of them belong to Mastigo- mycotina group, but none of zoopathogenic fungi were listed in this first pro- posal. (http://iasv.dbe.pmf.uns.ac.rs/index.php?strana=pocetak). Only limited reports examine the aquatic fungi in Serbia. The aquatic fungal community recorded in five large reservoirs of Serbia comprised mostly autochthonous species: Achlya americana, A. diffusa, A. racemosa, Dictyuchus sterile, Isoachlya toruloides, Leptomitus lacteus, Pythium ultimum, Saproleg- nia ferax, S. hypogyna, S. monica (R a n k o v i ć, 2005). Most of them were zoopathogenic. Leptomitus lacteus was reported to be pathogenic for the fish spawn (K i z i e w i c z, 2004), and Achlya americana and Saprolegnia ferax, were proven to be pathogenic for some fish species (C h a u h a n et al., 2012), while Achlya racemosa, Dictyuchus sterile, and Saprolegnia ferax, had 100% frequency of occurrence amongst the infected fish (O g b o n n a and A l a b i, 1991). Crayfish plague outbreaks were characterized by mass mortalities of noble European crayfish without any apparent effects on other aquatic organisms. Crayfish trade and fishing activities spread the plague throughout Eu- rope covering most of the European countries (E d e r, 2004; K o z u b í k o v á et al., 2006; S o u t y-G r o s s e t et al., 2006; V r å l s t a d et al., 2011b). Ac- cording to A l d e r m a n (1996), crayfish plague broke out through the Dan- ube River to the territory of Bačka and Banat (today A.P. Vojvodina, the Re- public of Serbia) in 1879, and spread to the Drava River basin in 1881 (today Croatia). Until 1880, the disease spread through the Sava River to the northern Bosnia (today Republika Srpska), all to the Slovenian territory (1885). From 1955 until1970, almost all territories of Republika Srpska and Republic of Serbia were afflicted with the crayfish plague disease (Table 5). Mostly due to the spread of crayfish plague, significant declines occurred in the range of Astacus astacus species: approximately 52% decline was recorded in England for 10 years, 52% decline in France between 1995 and 2003, and 99.5% decline was estimated for a ten year period in the South Tyrol region of Italy. These countries were once greatly abundant with this species. Since there is no information on the rate of decline for all the countries in this species range, the situation in Republika Srpska and Serbia is likely to be simi- lar to that seen in France and Italy as the main threats, alien crayfish species

347 and Aphanomyces astaci, are present throughout much of this species range. This species is estimated to have undergone a 50-80% decline over a 10 year period over its global range. Sibley (2002) has suggested that in case that the current trend in the decline of this species continues, it will face possible extinction in Britain within the period of 30 years (http://www.iucnredlist.org/ details/2430/0). According to IUCN criteria (Version 3.1), the degree of endangerment of A. astacus in Serbia was evaluated as “Endangered” (“EN”), which was a higher degree than the international level determined for this species, i.e., “Vulnerable” (“VU”). (S i m i ć et al., 2008).

Tab. 5. – Available data on alien invasive species Aphanomyces astaci in Republika Srpska (Bosnia and Herzegovina) and in the Republic of Serbia

Country Recent Source finding http://www.oie.int/wahis_2/public/wahid.php/Diseaseinformation/ statusdetail Bosnia and – http://www.iucnredlist.org/details/153745/0 Herzegovina A l a g i ć 2009 A l d e r m a n, 1996 Republika http://www.oie.int/wahis_2/public/wahid.php/Diseaseinformation/ Srpska statusdetail A l d e r m a n, 1996 http://www.oie.int/wahis_2/public/wahid.php/Diseaseinformation/ Republic statusdetail of Serbia http://www.iucnredlist.org/details/153745/0 A l d e r m a n, 1996

CONCLUSION

Non-native alien zoopathogens have had a profound impact on the health of aquatic zoobiota in Republika Srpska and Republic of Serbia as well as around the region and the world as a whole. Crayfish plague (Aphanomyces astaci) broke out through the Danube River to the territory of Bačka and Banat (today A.P. Vojvodina, the Republic of Serbia) in 1879. Until 1880, the disease spread through the Sava River to the northern Bosnia (today Republika Srpska). From 1955 until 1970, almost all territories of Republika Srpska and Republic of Serbia were afflicted with the crayfish plague disease. Despite of the fact that the problems of the spread of crayfish plague in the territory of the Republika Srpska and Republic of Serbia have been of great significance, there is little data available for analyzing this issue. According to IUCN criteria, and mostly due to the Aphanomyces astaci invasion, the degree of endangerment of noble crayfish in Serbia was evaluated as “Endangered”, which was a higher degree than the international level determined for this species, i.e., “Vulnerable”.

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353 ИНВАЗИВНЕ ЗООПАТОГЕНЕ MASTIGOMICOTINA У РЕПУБЛИЦИ СРПСКОЈ, СРБИЈИ И СУСЕДНИМ ЗЕМЉАМА СА ПОСЕБНИМ ОСВРТОМ НА APHANOMICES ASTACI Слободанка Б. Вујчић1, Свјетлана Б. Лолић2, Мара М. Бојић3, Предраг Б. Илић4, Милана С. Новаковић5, Маја А. Караман5, Милан Н. Матавуљ5 1 Универзитет за пословне студије, Бања Лука, Република Српска 2 Природно-математички факултет, Департман за биологију, Универзитет у Бањој Луци, Република Српска 3 Фонд за заштиту животне средине Републике Српске, Бања Лука, Република Српска 4 Институт за заштиту животне средине, екологије и информатике, Бања Лука, Република Српска 5 Департман за биологију и екологију, Природно-математички факултет, Универзитет у Новом Саду, Република Србија Резиме Алохтоне зоопатогене микрогљиве имају дубок утицај на здравље акватич них зообиота у Републици Српској и Републици Србији, као и широм региона и света у целини. Зоонозе које изазивају микрогљиве широм света угрожавају ра зличите организме, и та претња се интензивира са повећањем глобалног тран спорта робе, људи и животиња. Миколози и они који се на овај или онај начин баве гљивама располажу са релативно мало информација о карактеристикама ин вазивних, зоопатогених гљива, јер једна паразитска врста гљива може да насе љава различите организме, и може бити патогена за неке од ових домаћина, али не и за друге. Узрочник куге нашег племенитог рака (акватична плесан Aphanomyces astaci) доспео је 1879. године Дунавом на територију Бачке и Баната (данас АП Војводина, Република Србија). Реком Савом болест се већ до 1880. године про- ширила територијом северне Босна (данас Република Српска, БиХ). Од 1955. до 1970. год. готово целокупну територију Републике Српске и Републике Србије освојила је ова зооноза. Упркос великом значају проблема ширења ракове куге на територији Републике Српске и Републике Србије, мало је доступних података који се баве овим питањем. Према IUCN критеријумима, углавном због инвазије Aphanomices astaci степен угрожености врсте племенитог рака у Србији се оце њу је као „угрожена”, што је за степен више од међународног нивоа утврђеног за ову врсту, тј. „рањива”. КЉУЧНЕ РЕЧИ: микрогљиве, инвазивне, Aphanomices astaci, Република Српска, Република Србија

ACKNOWLEDGMENTS

This work is part of the Project No. 114-451-2721/2012-02; supported by The Secretariat for Science and Technological Development of the Autonomous Province of Vojvodina (the Republic of Serbia).

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