Hirudinea as vectors and disease agents in fish
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Preferred Scientific Name
- Hirudinea as vectors and disease agents in fish
Pathogen/sTop of page
OverviewTop of page
Leeches are the only important fish pathogens in the phylum Annelida. Both freshwater and marine leeches have worldwide distribution and they occur in a diversity of habitats. Leeches can potentially affect the health of fishes in a variety of ways. Their most important role is as vectors of potentially pathogenic organisms. Both freshwater and marine leeches are known to transmit haemoflagellates of the genera Trypanosoma and Cryptobia (= Trypanoplasma) and the intracellular haemogregarines and piroplasmas to fish. There is accumulating evidence that leeches can also transmit viruses and bacteria. In addition, leeches may affect the host by the sheer amount of blood withdrawn during feeding. The feeding or attachment wounds caused by leeches may also serve as sites for secondary pathogenic invaders.
Aquatic leeches also serve as second intermediate hosts for Digenea, harbouring metacercariae of a number of different species. Most of these worms are adults in waterfowl, but some mature in freshwater fishes. However, none of these Digenea has been implicated in pathology of fishes so they are not considered further. Additional information on the role of leeches as intermediate hosts is in Sawyer (1986) or papers by Vojtek et al. (1967), Spelling and Young (1986a, b, c) and McCarthy (1990).
Extensive reviews on the general biology of leeches have been published (Mann, 1961; Sawyer, 1986). Pathological implications of marine leeches have been reviewed by Rohde (1984), and the role of leeches in the pathology of fish cultured in the tropics has been reviewed by Kabata (1985).
Leeches can be directly pathogenic to fishes, especially if conditions allow close, continuous contact between large numbers of leeches and their hosts. Thus, the presence of leeches in aquaculture facilities should always be cause for concern. However, the most important role of aquatic leeches is as vectors of pathogenic organisms. The study of leeches as vectors of pathogenic viruses and bacteria is still in its infancy and should be a productive area of research in the future. Even though the role of leeches as vectors for the various haematozoa groups is now well documented, vectors have been identified for only a very few of the myriad species known to inhabit the blood of fishes, especially for the intraerythrocytic protozoa. Current knowledge suggests that in a given area only one or two leech species transmit a wide variety of blood parasites, but vectors are known for so few haematozoa that this may not be a valid conclusion.
One of the intriguing questions remaining to be answered is the vector specificity of fish haematozoa. It has been generally assumed that vector specificity is high and that a haematozoan species utilizes only a single leech species as a vector. However, this assumption is contradicted by Cryptobia borreli, which appears to utilize two vectors that belong to different families, Hemiclepsis marginata, a glossiphoniid, and Piscicola geometra, a piscicolid. Rigorous comparative studies are needed to confirm the vector relationships of both P. geometra and H. marginata and to ascertain that they are transmitting the same species of flagellates. Experimental studies with frog and turtle trypanosomes (Siddall and Desser, 1992b) identify multiple leech vectors, although in both cases one of the leech species appears to be a more important vector than the other species. These results raise many interesting questions about the evolution of the vector-parasite relationships.
There are regions with an abundant leech and haematozoa fauna where important research could be conducted to determine if fish haematozoa species can be transmitted by more than one leech. For example, developmental stages of various haematozoa were reported from many different leech species in Newfoundland (Khan et al., 1991), but experiments are necessary to demonstrate whether other leeches can actually transmit haematozoa known to utilize Johanssonia arctica as a vector. Similar experiments should be conducted to determine whether Myzobdella lugubris can also transmit haematozoa known to utilize Calliobdella vivida in estuaries of the south-eastern USA. It is disappointing that few studies have been conducted on the vector role of fish leeches over the last decade.
With the advent of molecular phylogenetic techniques, an emerging area of interest is phylogenetic analysis of leeches. Recent studies have already suggested that leeches are just specialized oligochaetes (Siddall et al., 2001) and have also questioned some of the traditional classification based on morphology. Increased taxon sampling is needed before revised classifications can be proposed, but such studies are under way. Phylogenetic studies have resulted in an increased interest in fish leech taxonomy and recent studies have reported new species, even in areas that were thought to be well studied (e.g. Bielecki, 1997; Burreson and Rowehl, 2004). Unfortunately, the fish leech fauna in many parts of the world is still poorly known. Our knowledge is especially inadequate for the marine fauna of the southern hemisphere, but, even in areas where the fauna is relatively well known, taxonomic confusion persists (Barta and Sawyer, 1990).
[Derived from: Woo, PTK, ed., 2006. Fish diseases and disorders, Volume 1: Protozoan and Metazoan infections. (2nd edition) Wallingford, UK: CAB International]
Host AnimalsTop of page
Hosts/Species AffectedTop of page
Leeches that parasitize fishes are primarily in the families Glossiphoniidae and Piscicolidae. Glossiphoniid leeches occur on a wide variety of freshwater fishes, as well as other freshwater aquatic vertebrates. Piscicolid leeches occur on both freshwater and marine fishes.
DistributionTop of page
Freshwater fish leeches are most abundant in temperate lakes, ponds and streams, and occur worldwide on all continents except Antarctica. Marine leeches are known from all seas, but are most abundant in polar to temperate regions. They occur primarily on demersal species of all major fish groups, including lampreys, elasmobranchs and teleosts.
Distribution TableTop of page
The distribution in this summary table is based on all the information available. When several references are cited, they may give conflicting information on the status. Further details may be available for individual references in the Distribution Table Details section which can be selected by going to Generate Report.Last updated: 10 Jan 2020
|Continent/Country/Region||Distribution||Last Reported||Origin||First Reported||Invasive||Reference||Notes|
|Union of Soviet Socialist Republics||Present|
|-Newfoundland and Labrador||Present|
|-New South Wales||Present|
|Atlantic - Northeast||Present|
|Atlantic - Northwest||Present|
|Mediterranean and Black Sea||Present|
|Pacific - Northeast||Present|
PathologyTop of page
Clinical signs and gross pathology
Leeches alone are generally not considered important fish pathogens. Effects are usually localized and restricted to attachment and/or feeding sites on the skin, fins, gills or mouth. The muscular caudal sucker used for attachment usually causes little damage; however, leeches that are semi-permanent parasites may elicit a substantial host tissue response at the attachment site. Rhynchobdellid leeches feed on host blood or tissue fluid by means of a protrusible proboscis, which is inserted into host tissue and this feeding activity may produce localized petechial haemorrhage (Sloan et al., 1984; Jones and Woo, 1990b). Even though pathology is usually localized, heavy infestations can result in severe epidermal erosion and even mortality because of large amounts of blood loss or secondary effects of multiple feeding wounds. Thus, large numbers of leeches in aquaculture facilities should always be a cause for concern. Fish can tolerate a high burden of leeches with little apparent effect, but pathology may depend on the relative size of the leech compared with the fish. Kabata (1985), without providing details, reported that the presence of 100 leeches on a single fish in Africa resulted in no serious harm to the host. Other reports, however, suggest that leeches may be pathogenic or provide portals of entry through their feeding or attachment wounds for secondary pathogens. For example, general statements by Bauer (1961), Markevich (1963) and Bauer et al. (1973) suggest that Piscicola geometra can severely affect carp and other species in rearing ponds in Eastern Europe by causing severe emaciation, small bleeding ulcers and secondary invasion by bacteria and fungi.
One of the earliest accounts of a leech causing mortality is the report by Badham (1916) involving the leech Austrobdella translucens and the sand whiting, Sillago ciliata, in Australia. A few dozen whiting were periodically stocked with other species in a salt-water pond over a number of years and on each occasion the whiting were killed by the leeches. The fish developed large ulcerated patches on the skin and badly infested fish harboured asmany as 100 leeches on the fins and body surface. A. translucens was specific for sand whiting and other species of fish in the pond apparently survived well, suggesting that mortality of whiting was not the result of unfavourable water quality but from the effects of the leeches.
Leeches have recently been implicated in pathology of tank-reared orange-spotted grouper, Epinephelus coioides, in the Philippines. Heavy infestations of Zeylanicobdella arugamensis occurred in multiple patches of several hundred leeches on and at the bases of the fins and in the skin folds of the lower jaw (Fig. 4). The affected fish had multiple areas of haemorrhage and hyperplasia at attachment and feeding sites (Cruz-Lacierda et al., 2000), but there was no report of mortality.
Fig. 4. Heavy infestation of Zeylanicobdella arugamensis on cultured orange-spotted grouper in the Philippines. A. Entire fish showing clusters of hundreds of leeches (arrows). B. Close-up of the anal fin of fish shown in A illustrating masses of leeches (arrows). Photos courtesy of Erlinda Cruz-Lacierda, South-East Asian Fisheries Development Center, Iliolo, Philippines.
There have been a number of reports of leeches causing pathology in feral freshwater and estuarine fishes in North America. An epizootic of Piscicola punctata caused pathology in the bigmouth buffalo, Ictiobus cyprinellus, in the Rock River near Rockford, Illinois, USA (Thompson, 1927). During February and March of 1926, almost every fish was heavily infested with the leech; intensity ranged up to 50 leeches per fish taken from the river channel, and over 100 leeches per fish collected from backwaters and sloughs. It is interesting that the leech had not been observed during the previous two winters, even though sampling had been intensive, and fishermen reported no similar infestation in the last 50 years. Leeches were removed by fishermen prior to delivery to the retail market, but the raw and bleeding scars around the attachment sites made the fish difficult to sell. There was no mention of host mortality in the report. Leeches left the fish by the end of March when water temperature increased above 0ºC. In late April fungal infections were observed on wounds apparently made by leeches. This leech outbreak was unusual, but there were no obvious, unusual environmental conditions known to be present that would have caused such an occurrence. Undoubtedly, a number of factors contributed to the greater than normal reproductive success and hence the high abundance.
Another unusual occurrence of fish mortality caused by leeches involved adult brook trout, Salvelinus fontinalis, and freshwater leeches in a small, shallow lake in Maine (Rupp and Meyer, 1954). During periods of hot weather, water temperature in the lake can become critically high and trout congregate around cooler underwater springs in shallow water. The congregating trout encouraged poaching and bird predation, so brush was placed in the lake to provide cover for the fish. Unfortunately, the brush provided an ideal habitat for two hirudinid leeches, Macrobdella decora and Haemopis grandis. These leeches are not normally associated with fish, but on one occasion 50 to 60 large trout were observed 'being fiercely attacked by hordes' of leeches from the brush. Despite continual harassment by the leeches, the trout remained congregated in the spring. On one occasion over 20 dead trout were reported during a 3-day period. One captured, dying trout had six leeches attached to the gill arches, isthmus and fin bases; one M. decora had rasped an opening through the body wall and into the ventral aorta. It appeared certain to the investigators that the fish was dying from loss of blood. This unusual occurrence was possible only because of high concentrations of fish and leeches in close proximity for prolonged periods.
Freshwater leeches have also caused mortality in fish hatcheries. A heavy infestation of Piscicola salmositica caused mortality as high as 25% in sac fry of pink salmon, Oncorhynchus gorbuscha, in the state of Washington (Earp and Schwab, 1954). Leeches invaded the hatchery through the freshwater supply from a nearby stream and attacked fry as they hatched in trays. Once attached to the fry, leeches quickly became gorged with blood and the fry invariably died, apparently from blood loss. Adult salmon migrants in the supply stream also had heavy infestations of P. salmositica and indications were that some fish died before spawning.
Leeches that are semi-permanent parasites on fishes, such as the freshwater and estuarine leech Myzobdella lugubris, tend to remain attached at a single site. They often cause very localized histopathological changes, including cellular infiltration, erosion of the integument under the attachment site and hyperplasia of the epidermis around the caudal sucker. Localized subcutaneous haemorrhages often occur at leech feeding sites. Paperna and Zwerner (1974) reported removing over 500 Myzobdella lugubris from a single moribund white catfish, Ictalurus catus, in the York River estuary in Virginia, USA. Leeches were in the mouth and under the operculum and externally on the skin fold behind the lower jaw and at the bases of the fins. Extensive histopathological changes caused by the leech included inflammation, displacement and erosion of the dermis and hyperplasia of the epithelium. All pathological changes were attributed to leeches and it was concluded that leeches were at least a major contributing factor to the distressed condition of the fish. The same leech was also implicated in an epidemic of oral ulcerations in adult largemouth bass, Micropterus salmoides, from Currituck Sound, North Carolina, USA (Noga et al., 1990). A systematic survey was not conducted, but sport fishermen reports suggested that 90% of legal-size fish might have been affected. These fish had large ulcerations on the tongue and buccal cavity, often extending to underlying musculature; leeches were always present in or near the wounds. Localized pathology from M. lugubris also has been reported in logperch, Percina caprodes, and brown bullhead, Ictalurus nebulosus, in Ontario, Canada (Appy and Cone, 1982), and in mullet, Mugil sp. (Paperna and Overstreet, 1981). Heavy infestations of Myzobdella lugubris were reported in intensive striped bass (Morone saxatilis) culture facilities on the Chesapeake Bay, Maryland, USA, but there was no mention of pathology (Woods et al., 1990).
Similar pathological effects caused by Austrobdella bilobata have been reported in yellowfin bream, Acanthopagrus australis, in New South Wales, Australia (Roubal, 1986). Khan (1982) described subcutaneous lesions caused by Johanssonia arctica in Atlantic cod, Gadus morhua.
Effects on host physiology
Leeches have only rarely been implicated as serious pathogens of fishes. Their effects are usually localized to the feeding or attachment sites and only become serious when infestation is high. Documented fish mortality caused by leeches is extremely rare and appears to occur only when there is close, prolonged contact between large numbers of leeches and fish. Although a single leech may withdraw only a small amount of blood, it nevertheless weakens the host (Meyer, 1946a). The subtle effect of blood loss was elegantly demonstrated by Mace and Davis (1972), who studied the energetics of parasitism by the leech Malmiana brunnea on the shorthorn sculpin, Myoxocephalus scorpius, in Newfoundland, Canada. Energy budgets were developed for leeches and fish, and growth was measured in two groups of unparasitized fish for 5 weeks. Growth of a parasitized group was significantly lower than the expected growth and the difference was attributed to the energy requirements of the leeches. It was concluded that the additional energy consumption of the host because of the leeches was approximately 750 cal/g of leech per week. According to Mace and Davis (1972), a well-adapted host-parasite relationship should exert a metabolic demand that is little more than the energy requirements of the parasite. However, tissue damage, harmful metabolites and/or hormone leakage cause increased energy loss. They concluded that energy loss in sculpins was not entirely because of the energy requirements of the leech, but probably also because of increased physiological strain from leech saliva secretions or undetected mechanical irritation of feeding leeches.
DiagnosisTop of page
Leeches can be difficult to collect and to identify. They often leave the host after feeding and, therefore, may go undetected even when abundance is high. They are usually sufficiently large to be detected by the naked eye and occur on the body surface and fins or in the gill cavity or mouth. If possible, leeches should be collected by gently dislodging the caudal sucker with forceps and placing them in a dish containing water. For proper identification it is important to observe leeches alive and to note as many external characters as possible. It may be necessary to relax leeches in weak alcohol or other narcotizing agent prior to examination. Careful observation should be made of pigmentation colour and pattern, number and arrangement of eyes on the oral sucker, ocelli on the body and caudal sucker, number of lateral pulsatile vesicles, if present, and arrangements of papillae, tubercles or other obvious external characters. Leeches that have been fixed unrelaxed are almost impossible to identify because they usually contract strongly or curl into a tight ball, making observation of important characters difficult. Leeches relaxed prior to fixation in formalin will usually retain their pigmentation and eyes for long periods; however, pigmentation fades rapidly after transfer to alcohol. Leeches that have been fixed and then preserved in alcohol are often difficult to identify, especially to species. Generic determination of many leeches, especially piscicolids, may depend on internal anatomy, which can only be determined with serial sections. All these difficulties combine to make identification of leeches, even for experts, problematic.
ReferencesTop of page
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