K. Molnar
Veterinary Medical Research Institute
Budapest, Hungary
ABSTRACT
Several new species of parasite have spread into Hungary as a consequence of fish transfers. Some of these parasites were brought in with introduced fish, while others, originating from fish introduced to the neighbouring countries, have actively invaded the country through natural waters. The parasite fauna has increased especially after the introduction of the E. Asian herbivorous fishes, which - apart from specific parasites also carried - several parasites which have also affected the native fishes. The probability of introducing pathogens during the transfer of older fish is very high, while in yolk-sac fry it is minimal. The spread of parasites cannot be stopped by country borders and so fish naturalizations bear international implications. After the several pathogenic parasite species have passed across natural barriers forming the borders of fauna systems, their spread, on appropriate host fishes, is only a matter of time.
RESUME
Plusieurs nouvelles espèces de parasites se sont propagées en Hongrie à la suite d'introductions de poissons, soit dans le pays même, soit dans des pays voisins dont les eaux communiquent avec celles de la Hongrie. La faune parasitaire s'est accrue, notamment après l'introduction de poissons herbivores, quand, outre les parasites spécifiques plusieurs parasites affectant également les poissons indigènes se sont établis dans les eaux hongroises. Le risque d'introduire des agents pathogènes lorsque l'on transplante des poissons assez âgés est très élevé; en revanche, il est minime avec des alevins dont le sac vitellin ne s'est pas encore résorbé. La propagation des parasites ne connaît pas de frontières et l'introduction de nouvelles espèces de poissons est donc une affaire internationale. Une fois que des parasites pathogènes ont franchi les barrières naturelles, leur propagation - en présence de poissons hôtes - n'est plus qu'une question de temps.
During the last hundred years several new fish species have become permanent members of the Hungarian fauna (Pinter, 1980). Some of these have reached the country by invasion, while others have been introduced. In most cases the fish also brought with them elements of their parasite fauna from their original biotope. The first detailed survey of introduced parasites took place after the translocation of herbivorous fishes to Hungary, when Szakolczai and Molnar (1966) reported the appearance of several parasites previously unknown in the country.
The simultaneous spread of fish parasites and their hosts is well documented in the literature and in the case of Asiatic herbivorous fishes and the Amur wild carp diffusion throughout the water system of Central Asia and Europe can be followed in the works of the Soviet researchers (Babayev, 1965; Bauer and Strelkov, 1972; Malevitskaya, 1958; Kulakovskaya and Krotas, 1961; Musselius, 1967 and Vismanis, 1962). Data concerning the transcontinental spread of the parasites of herbivorous fishes and salmonids in America (Hoffman, 1970; Bauer and Hoffman, 1976) and in New Zealand (Edwards and Hine, 1974) can also be found. Some of the introduced parasites proved to be highly pathogenic on their new biotope, causing animal health problems (Musselius, 1976; Molnar, 1970, 1972; Korting, 1974; Hoffman, 1980).
The present paper deals with the mode of introduction or spread of non-indigenous parasites into the country, and with the pathological significance of these parasites.
In our Institute we have continuously studied the parasite fauna of fish living in the natural waters and fish farms of Hungary since 1960. Apart from these zoological investigations, we have also carried out animal health inspections in some fish farms regularly, in others occasionally.
The fish studied were transferred alive to the laboratory where the parasites were collected by dissection under a microscope. Squash preparations and histological sections were examined for the presence of tissue parasites.
The first undoubtedly introduced parasites were found by Molnar (1963) on the brown bullhead (Ictalurus nebulosus), a fish transferred from the United States in 1902 and on the pumpkinseed (Lepomis gibbosus) which was transferred to Hungary in 1895. Monogeneans including Cleidodiscus pricei (Mueller, 1934), Haplocleidus dispar (Mueller, 1936) and Urocleidus similis (Mueller, 1936) collected from the gills of the above fishes proved to be typical North American species, and due to their relatively high host specificity these have not spread to the native fishes. Cleidodiscus pricei has only been found on the brown bullhead and on Ictalurus melas originating also from America, which were transferred to Hungary through Italy. In this case, it was not possible to decide whether the I. melas brought its parasites from Italy or acquired them from the previously acclimatized brown bullhead. The first alternative seems to be more likely, because there were no brown bullhead near the quarantined I. melas stock.
In 1963, large numbers of herbivorous fishes were transferred to Hungary from Chinese natural waters. Four species, grass carp (Ctenopharyngodon idella), silver carp (Hypophthalmichthys molitrix), bighead (Aristichthys nobilis) and Mylopharyngodon piceus were introduced to the country. A fifth species, Pseudorasbora parva was also introduced accidentally. Several parasite species were detected on the quarantined fish (Szakolczai and Molnar, 1966) some of which proved to be undoubtedly Far Eastern parasites. The majority of the species then detected are regular parasites of cultured herbivorous fishes even at the present time. Two species, the grass carp and the bighead were infected with monogeneans, among which Dactylogyrus lamellatus (Achmerov, 1952) and D. nobilis (Long and Yu, 1958) are specific parasites of the grass carp and the bighead, respectively. At the same time, Myxobolus pavlovskii (Achmerov, 1954) and the intestinal parasite Eimeria sinensis (Chen, 1956) proved to be common parasites of both the silver carp and the bighead. Cryptobia branchialis (Nie, 1956) found on the gill rakers and Spironucleus sp. living in the intestine, have established themselves on carp in addition to the herbivorous fishes. During the investigations carried out in 1963–64 two additional parasites of Far Eastern origin, a Myxidium sp. (Protozoa) and Amurotrema dombrovskajae (Achmerov, 1959) (Trematoda) were detected in herbivorous fishes, though these parasites have not been observed since then. On the other hand, no introduced parasites were found on Mylopharyngodon piceus and Pseudorasbora parva, which had been introduced only in small numbers.
During our investigations, particular attention was paid to Bothriocephalus acheilognathi (Yamaguti, 1934) syn. B. gowkongensis (Yeh, 1955) infection of the quarantined fish because according to Soviet authors this parasite was a dangerous pathogenic species. In spite of regular inspection, the parasite was detected five years after lifting the quarantine in both the naturalized fish and in carp kept with them. At the same time, Bothriocephalus infection was detected in an isolated minnow stock five months after naturalization. That this infection spread to this biotope by ten grass carp fry removed from quarantine was found out only several years later. After its detection B. acheilognathi became widely distributed in the country and is now one of the most significant pathogens in carp stocks.
Two more parasites, Trichophrya sinensis (Chen, 1955) a gill parasite of the silver carp and bighead, and Myxobolus drjagini (Achmerov, 1954) a head skin parasite of the former two species were also introduced as a latent infection with the first transport from China. The occurrence of these parasites was detected only a year after the naturalization of the fish.
Between 1964 and 1969 we imported artfically-hatched fry of herbivorous species from the U.S.S.R. These fishes did not bring any parasites with them and the parasite species originating from China caused infection only in those fish farms in which previously imported fish were kept.
The parasite fauna of the native herbivorous fishes was further enriched in 1966 when broodstocks were imported from the U.S.S.R. Numerous Balantidium ctenopharyngodonis were present (Chen, 1955) in the intestine of grass carp transported at that time, while numerous Datylogyrus ctenopharyngodonis (Achmerov, 1952) parasites were detected on their gills. Entamoeba ctenopharyngodoni had probably also spread into Hungary on this occasion (Chen, 1955) and was detected only later.
Only a few of the parasites introduced with herbivorous fishes have established themselves on native species (including Cryptobia branchialis, Spironucleus sp., Bothriocephalus acheilognathi). Of these, only the Bothriocephalus species has pathological significance.
Infection with Lernaea has been known in Hungary for a long time, but has gained pathological significance only since the naturalization of the herbivorous fishes. At the present time, we cannot decide merely on morphological grounds whether the increased pathogenic importance of lernaeosis can be attributed to the introduction of Lernaea elegans Leigh-Sharpe, 1925, or to the changed conditions arising from the expansion of polycultural fish rearing promoting the reproduction of the native Lernaes cyprinacea Linne, 1758.
An intensive introduction of fish from China and from the region of the River Amur to Romania and the European part of the U.S.S.R. had been carried out prior to the transport of herbivorous fishes to Hungary. These fish brought with them a considerably larger parasite fauna than to Hungary (Radulescu and Georgescu, 1962; Musselius, 1965). Owing to the common water system, these parasites will probably spread into Hungary sooner or later. Indeed, the appearance of Dactylogyrus suchengtaii (Gussev, 1962) a gill parasite of the silver carp in fish farms situated in the vicinity of the Romanian border already shows the capacity of such species to spread.
An eel parasite, Myxidium giardi Cepede, 1906, is brought into the country in large numbers with the annual import of elvers. This parasite cannot be demonstrated in older fish but considerable infections with Bothriocephalus claviceps (Goeze, 1782) can be detected in the intestine of the more developed eels. Fortunately, eel bothriocephalosis does not affect other fish species.
The fact that up to now we have failed to detect specific parasites on Carassius auratus gibelio introduced to Hungary in 1954 and on Neogobius fluviatilis, which appeared in Lake Balaton in 1970, is remarkable since these fishes possessed a rich parasite fauna in their original biotopes.
Fish transfers have also had indirect negative effects which increasingly make themselves felt in Hungary. There have been no wild carp introductions into Hungary from the Far East or Eastern Europe. In spite of this, several common carp parasites are supposed to have spread into Hungary through rivers from the U.S.S.R. and Romania. Ivasik and Karpenko (1967) reported that Amur wild carp (Cyprinus carpio haematopterus) had been first transferred in 1955 from the River Amur to the Ukraine, which borders on Hungary. These fish brought with them three parasites previously unknown in Europe, Myxobolus amurensis Achmerov, 1960; Khawia sinensis Hsu, 1935, and Philometroides lusiana (Vismanis, 1962), which established themselves on the local mirror carp.
In addition to the parasites listed above, presumably other species have also appeared in the Ukraine, from whence some carp parasites of Far Eastern origin have already spread into Hungary either directly or through Romania. Among these, the gill parasite Dactylogyrus achmerowi Gussev, 1955 and the tapeworm Khawia sinensis have been detected in Hungary for the first time, but recently Thelohanellus nikolskii Achmerov, 1955 and T. hovorkai Achmerov, 1960, have also been demonstrated.
The above-mentioned parasite species have obviously spread to our fish farms on carp living in natural waters, and among them Khawia sinensis and Thelohanellus nikolskii already have an undoubted economic significance.
A regular treatment is applied for the control and eradication of the introduced tapeworms in the Hungarian pond farms which is included in the standard technology. Many regulations concerning the disinfection of fish ponds have also been necessary to destroy the introduced spore-bearing parasites.
Parasitological analysis of the European and, primarily Hungarian, fish transfers has proved that during fish transfers which lack the advice of expert pathologists, the transported fish may carry numerous parasites from remote biotopes to the site of naturalization. Among these parasites many keep on causing damage to their hosts in their new biotope. This is a relatively negligible factor since calculations concerning the probable usefulness of a fish species include not only its favourable properties but also its proneness to the diseases affecting it. Those parasites cause problems in the first place which affect not only the introduced fish species but also the native fishes. These include the species of loose host specificity which can live on several fish species, e.g., Bothriocephalus acheilognathi, which affects all carp species.
There are significant differences among the parasite groups as to the probability of naturalization of the introduced parasites. Those parasites which spread directly from fish to fish and can multiply even on the same individual, e.g., flagellates, or those which develop on the bottom for a short time, e.g., gill parasites, have great advantages because a single introduced parasite can eventually infect a whole fish stock. Rapid spread may be expected also in spore-bearing protozoans, where, if the introduced fish species is bred on the same water area in the following year, fish of the new generation will be able to ingest the spores of the parasite which generally has a seasonal developmental cycle, (e.g., Myxobolus drjagini). Experience proves that parasites requiring an intermediate host can also multiply if the proper organism is common in the new environment for example, cyclops in the case of Bothriocephalus or tubifex in the case of Khawia. On the other hand, the naturalization of the trematode species Amurotrema dombrovskajae has obviously been prevented by the lack of the proper molluscan intermediate host.
During introduction of broodstock even the most careful quarantine fails to assure freedom from parasites and most parasites characteristic of the fish species have the possibility of spreading to the new biotope. The situation is similar in the case of the already feeding fry though these sometimes bring along with them only those diseases characteristic of the young fish. The introduction of the grass carp to Hungary may serve as an appropriate example. Knowing the biology of the parasite Dactylogyrus ctenopharyngodonis and Balantidium ctenopharyngodonis, which are characteristic parasites of older fish, have spread into Hungary with the broodstock and not with the fry. Thus herbivorous fishes brought into the country as yolk-sac fry remained free from specific parasites as long as they had not come into contact with the generations introduced earlier. If we consider the cost of medication and labour necessary for the control of bothriocephalosis and gill parasitosis of grass carp, the saving of one year by the introduction of the first infected stock from China was not worthwhile. If this introduction had not taken place, we could have hoped to maintain a relatively parasite-free herbivorous fish stock in Hungary for some considerable time.
This supposition is, of course, not wholly true because fish naturalizations exert their influence not according to country borders but through water systems and the spread of both host and parasite along water courses cannot be stopped by even the most radical animal health regulations. thus, fish introductions have international significance, and if these occur across geographical barriers they will always be followed by unfavourable consequences.
During his studies on monogeneans Gussev (1969) distinguished five faunal complexes in Eurasia. It is known that the parasite fauna of the amuro-sino faunal complex is much richer than that of the palaearctic region in which Europe is located (Achmerov, 1952; Gussev, 1955; Ivasik, 1968 and Ergens, 1969), and Europe has already become partly acquainted with this rich fauna, which has been a severe lesson. We can only hope that ichthyologists and fish culturists will profit from these unfavourable experiences and will organize fish naturalizations more circumspectly, choosing to introduce eggs and fish larvae rather than adult fish. In this case, there is hope that fihs species of high productivity will maintain their freedom from parasites in their new biotope and will not endanger the health of the native fish fauna.
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