Ichthyophthirius multifiliis Fouquet and Ichthyophthiriosis in Freshwater Teleosts

https://doi.org/10.1016/S0065-308X(05)59003-1Get rights and content

Abstract

The ciliate Ichthyophthirius multifiliis is an important pathogen of freshwater teleosts occurring in both temperate and tropical regions throughout the world. The disease, ichthyophthiriosis, accounts for significant economic losses to the aquaculture industry, including the ornamental fish trade, and epizootics in wild fish populations can result in mass kills. This review attempts to provide a comprehensive overview of the biology of the parasite, covering the free-living and parasitic stages in the life cycle, host–parasite interactions, and the immune response of host and immune evasion strategies by the parasite. Emphasis on the immunological aspects of infection within the fish host, including molecular studies of i-antigens, reflects the current interest in this subject area and the quest to develop a recombinant vaccine against the disease. The current status of methods for the control of ichthyophthiriosis is discussed, together with new approaches in combating this important disease.

Introduction

The ciliate Ichthyophthirius multifiliisFouquet, 1876, commonly called ‘ich’ (pronounced ‘ik’), is probably the most widespread parasite of freshwater teleosts with a geographical range extending from the tropics to temperate regions, northwards in Europe to the Arctic Circle. The first records of the characteristic ‘white spots’ in fish, which mark the location of the parasite in the skin (Figure 1), were from China before ad 1126 (Dashu and Lien-Siang, 1960). These observations support the view that I. multifiliis was originally endemic in the Far East, being introduced to Europe in the Middle Ages with the development of carp culture (Hoffman, 1970b) and to many other countries, including the United States, through the importation of goldfish, Carassius auratus (see Hoffman (1970a), Hoffman (1978)). The parasite was probably introduced to South Africa in the 18th century with importation of carp (Huchzermeyer, 1994; Mouton et al., 2001), this fish now being established in temperate waters of the continent (De Moor and Bruton, 1988). Paperna (1972), Paperna (1991) has reviewed the occurrence of I. multifiliis in warmer regions of the world. Key factors in the current worldwide distribution of I. multifiliis in freshwater teleosts, including cold water and tropical species, are wide temperature tolerance together with low degree of host specificity and direct life cycle. In the Far East, I. multifiliis is well adapted to survive the seasonal changes in temperature (4 to 28°C) experienced by its common host, Cyprinus carpio. Nigrelli et al. (1976) considered the possibility of multiple physiological races and even different species of Ichthyophthirius, adapted to different temperatures. Two new species of ‘ich’-like parasites have been described, namely, Ichthyophthirioides browniRoque and de Puytorac, 1968 and Neoichthyophthirius scholtfeldtiBauer and Yunchis, 2001 from tropical fish; however, strains or races of I. multifiliis based upon physiochemical characters have yet to be defined. Dickerson et al. (1993) have demonstrated serotypic variation among isolates of the parasite, which they suggested could find application as biochemical markers in strain identification and in epidemiological studies of the parasite. Recent studies by Aihua and Buchmann (2001) on the development of a Nordic isolate of I. multifiliis provided a valuable approach to defining strains, based on physiological features of the free-living stages in the life cycle.

The disease ichthyophthiriosis, or ‘white spot’, probably accounts for more damage to freshwater fish populations worldwide than any other eukaryote pathogen (Hines and Spira, 1973a; Rogers and Gaines, 1975). Aquarists have been aware of the condition in ornamental species since the turn of the century, associating mortalities with the appearance of the white spots within the skin and gills. Today, ichthyophthiriosis is a significant factor not only in the freshwater ornamental industry but also in the intensive farming of salmonids (Valtonen and Keränen, 1981; Wahli and Meier, 1987), carp (Hines and Spira, 1973a; Körting, 1984), channel catfish (Klesius and Rogers, 1995), eels (Egusa et al., 1970), and Tilapia species (Subasinghe and Sommerville, 1986). Although epizootics have been less frequently observed in wild fish populations, they are usually associated with mass kills (Elser, 1955; Allison and Kelly, 1963; Kozel, 1976; Wurtsbaugh and Tapia, 1988) following recent introduction (Hoffman, 1970b). Nevertheless, that the disease can have a significant impact on commercial fisheries is indicated by a more recent outbreak in pre-spawning and spawning sockeye salmon, when an estimated 153.6 million fewer fry were produced as a result of ichthyophthiriosis (Traxler et al., 1998).

I. multifiliis has been used as a model in fundamental studies of fish behaviour and fish immunology. Milinski and Bakker (1990) used the parasite to investigate the function of secondary sexual ornamentation in teleosts. They found that infections influenced female choice of partner in stickleback populations, the white spots associated with the parasite in the epidermis reducing the intensity of male red breeding coloration. Dickerson et al. (1997) and Dickerson and Clark (1998) have discussed the development of I. multifiliis as an experimental system for the investigation of cutaneous immunity in fish.

MacLennan (1935a) and Butcher (1943) provided interesting accounts of the early studies on the life cycle of I. multifiliis, later work on the subject being reviewed by Matthews, R.A. (1994) and Dickerson and Dawe (1995). I. multifiliis is an endoparasite in which the trophont, or feeding stage, occurs within the epidermis of the fish host. The life cycle is direct (Figure 2). The trophont, following a period of growth and development, transforms to the tomont, which actively leaves the host tissues, encysting within the aquatic environment. The tomont undergoes a rapid phase of division, normally within the cyst, with the production of daughter cells called tomites. Following a set number of divisions each tomite differentiates into a theront, the stage infective to the fish host.

According to Fouquet (1876), Hilgendorf and Paulicki were probably the first to publish (in 1869) details concerning both the morphology and life history of I. multifiliis, noting somatic cilia, macronucleus, contractile vacuoles and granules, and that the trophont stage leaves the fish host to encyst and undergo reproduction as a free-living stage. Although they had suggested that the ciliate might be related to Opantotricha Ehrenberg, Fouquet (1876) proposed the name I. multifiliis for this parasite, the specific name relating to the large number of daughter cells (tomites) produced at encystment. Fouquet (1876) described the parasite from juvenile trout, noting further details of morphology including mucocysts and cytopharynx. The oral ciliature, as described by Roque et al. (1967), forms the basis for the inclusion of I. multifiliis within the class Oligohymenophorea. The relationship of I. multifiliis to other histophagous parasites of fish within the Hymenostomatida is shown in Figure 3. Canella (1964) established the suborder Ophryoglenina to include all species with an organelle of Lieberkühn, this structure being recognized as an important taxonomic feature. Lynn et al. (1991) confirmed the suborder as a monophyletic taxon following ultrastructural investigations of the organelle within the tomont of Ophryoglena sp. and theront of I. multifiliis. Separation of Ophryoglenina from Tetrahymenina is clearly supported by studies of ciliate phylogeny based upon the characterization of the histone H3/H4 gene region (Van den Bussche et al., 2000) and similarities in small subunit rRNA gene sequences (Wright & Lynn (1995), Wright & Lynn (1997); Hammerschmidt et al., 1996). The family Ichthyophthiriidae Kent, 1881 was erected solely for I. multifiliis; the status of Ichthyophthirioides browni has still to be confirmed, as there has been no further record of the species since its description by Roque and de Puytorac (1968). Cryptocaryon irritans, the cause of white spot in marine fish, is no longer included within Hymenostomatidae (Diggles and Adlard, 1995; Wright and Colorni, 2002). Similarities with Ichthyophthirius multifiliis concerning life cycle and course of infection are attributed to parallel evolution. Recently, Wright and Colorni (2002) sequenced the complete 18S rRNA gene of C. irritans and on the basis of phylogenetic analysis have re-assigned this parasite to the class Protostomatea, erecting a new family, Cryptocaryonidae, within the order Prorodontida.

Section snippets

Behaviour and encystment

The tomont culminates the growth phase within the fish host (Figure 2), attaining a size and stage of development sufficient to complete the aquatic phase, including location of substrate, encystment and production of viable theronts (Ewing and Kocan, 1992). This free-swimming stage encysts within 15 min to 6 h of leaving the host fish epidermis (MacLennan, 1937). Nickell and Ewing (1989) demonstrated a marked photoresponse to substrate colour, significantly larger numbers encysting on light

Invasion of the Fish Epidermis

Although there have been many observations concerning the entry of I. multifiliis into the epidermis of host fish, there is little agreement concerning the mechanism involved (Matthews, R.A. 1994). MacLennan (1935b), in the first major work on the parasite, considered that the theront bored into the epidermis using ‘the non-ciliated anterior region’ as a wedge to force the tissues apart, noting that ‘the closely set cilia are more powerful and active than those of the average ciliate’. Roque et

Trophont

Transformation from theront to trophont is characterized by discharge of mucocysts, disappearance of the organelle of Lieberkühn, enlargement of the cytopharynx, and the onset of phagocytosis. These events are completed within 12 h in primary infections of juvenile carp at 20°C (Matthews, R.A., et al., 1996).

i-Antigens

Dickerson and Clark (1996) provided an excellent review of their pioneering studies of immobilization (i-) antigens in I. multifiliis. Lin and Dickerson (1992) were the first to identify and characterize i-antigens in this parasite using an isolate (G1) from tropical fish purchased in Georgia, USA and maintained through serial passage in Ictalurus punctatus (see Dickerson et al., 1989). They isolated polypeptides of 48 and 60 kDa from a single serotype A, designated G1 (serotype A), with the

Ichthyophthiriosis

Hines & Spira (1973a), Hines & Spira (1973b), Hines & Spira (1974a), Hines & Spira (1974b), in their seminal works on I. multifiliis, provided a comprehensive account of the pathogenesis of ichthyophthiriosis in carp covering aspects of immunopathology and pathophysiology. Ventura and Paperna (1985) have undertaken a detailed histopathological investigation of the disease in the skin and gills in a range of fish hosts, including carp. Further studies have also focused on events within the skin

Control and Treatment

Control of ichthyophthiriosis, like that of other parasitic diseases, requires an integrated approach based upon knowledge of aetiology and epidemiology. In temperate regions, disease risk forecasting by monitoring water temperatures in spring and early summer would provide some warning of impending epizootics and ensure a more targeted approach in the application of control measures. The prevalence of I. multifiliis is known to fluctuate with season (Dickerson and Dawe, 1995). In central

Conclusion

Significant advances have been made in our knowledge of I. multifiliis since reviewing the parasite in 1994 (Matthews, R.A., 1994). Notable achievements include the characterization of serotypes, the isolation of genes expressing i-antigens, and the successful insertion of one of these genes into Tetrahymena thermophila, affording a way forward for the development of recombinant vaccines against ichthyophthiriosis. Immunological studies have led to a better understanding of the protective

Acknowledgement

This review would not have been possible without the support of my wife, Dr Ben Matthews. I thank her for her patience and valuable advice throughout its preparation, and for providing the electron micrographs.

References (290)

  • K.B. Davis et al.

    Effect of handling stress on susceptibility of channel catfish Ictalurus punctatus to Ichthyophthirius multifiliis and channel catfish virus infection

    Aquaculture

    (2002)
  • K.B. Davis et al.

    Effect of dietary cortisol on resistance of channel catfish to infection by Ichthyophthirius multifiliis and channel catfish virus disease

    Aquaculture

    (2003)
  • H.W. Dickerson et al.

    Immune response of fishes to ciliates

    Annual Review of Fish Diseases

    (1996)
  • M.S. Ewing et al.

    Invasion and development strategies of Ichthyophthirius multifiliis, a parasitic ciliate of fish

    Parasitology Today

    (1992)
  • L. Aihua et al.

    Temperature- and salinity-dependent development of a Nordic strain of Ichthyophthirius multifiliis from rainbow trout

    Journal of Applied Ichthyology

    (2001)
  • D.J. Alderman

    Malachite green: a review

    Journal of Fish Diseases

    (1985)
  • K.O. Allen et al.

    Effects of brackish water on ichthyophthiriasis of channel catfish

    The Progressive Fish-Culturist

    (1970)
  • R.D. Allen

    Paramecium phagosome membrane; oral region to ectoproct and back again

    Journal of Protozoology

    (1984)
  • R.D. Allen et al.

    Membrane dynamics of the contractile vacuole complex in Paramecium

    Journal of Protozoology

    (1988)
  • R. Allison et al.

    An epizootic of Ichthyophthirius multifiliis in a river fish population

    The Progressive Fish-Culturist

    (1963)
  • E. Amlacher

    Textbook of Fish Diseases

    (1970)
  • J. Antychowicz et al.

    Scanning electron microscopic studies on Ichthyophthirius multifiliis infection in the skin of carp (Cyprinus carpio)

    Bulletin of the Veterinary Institute of Pulawy

    (1992)
  • Areerat, S. (1974). The Immune Response of Channel Catfish, Ictalurus punctatus (Rafinesque), to Ichthyophthirius...
  • O.N. Bauer

    Biologie und Bekämpfung von Ichthyophthirius multifiliis Fouquet

    Zeitschrift für Fischerei und deren Hilfswissenschaften

    (1958)
  • O.N. Bauer et al.

    A new genus of parasitic ciliata from tropical fishes

    Parazitologiya

    (2001)
  • O.N. Bauer et al.

    Diseases of Pond Fishes

    (1973)
  • H. Beckert et al.

    Some host response of white catfish to Ichthyophthirius multifiliis (Fouquet)

    Proceedings of the South-eastern Association of Game and Fish Commissioners

    (1964)
  • Bills, T.D., Marking, L.L. and Chandler, J.H., Jr. (1977). Malachite green: its toxicity to aquatic organisms,...
  • Y. Bisharyan et al.

    Cadmium effects on Ichthyophthirius: evidence for metal-sequestration of fish tissues following administration of recombinant vaccines

    Parasitology

    (2003)
  • L.R. Bodensteiner et al.

    Flowing water: an effective treatment for ichthyophthiriasis

    Journal of Aquatic Animal Health

    (2000)
  • P. Borst et al.

    Antigenic variation in African trypanosomes

    Science

    (1994)
  • G.B. Bouck et al.

    Synthesis and assembly of flagellar surface

    Journal of Protozoology

    (1984)
  • E.M. Brown et al.

    Fish Farming Handbook. Food, Bait, Tropicals and Goldfish

    (1980)
  • C.F. Brunk

    Ciliates display promise for foreign gene expression

    Nature Biotechnology

    (1999)
  • K. Buchmann et al.

    Partial cross protection against Ichthyophthirius multifiliis in Gyrodactylus derjavina immunised rainbow trout

    Journal of Helminthology

    (1999)
  • K. Buchmann et al.

    Effects of sodium percarbonate and garlic extract on Ichthyophthirius multifiliis theronts and tomocysts: in vitro experiments

    North American Journal of Aquaculture

    (2003)
  • K. Buchmann et al.

    Effects of formalin treatment on epithelial structure and mucous cell densities in rainbow trout, Oncorhynchus mykiss (Walbaum), skin

    Journal of Fish Diseases

    (2004)
  • P.J. Burgess et al.

    Cryptocaryon irritans (Ciliophora): photoperiod and transmission in marine fish

    Journal of the Marine Biological Association of the UK

    (1994)
  • M.A. Burkart et al.

    Immunization of channel catfish, Ictalurus punctatus Rafinesque, against Ichthyophthirius multifiliis (Fouquet): killed versus live vaccines

    Journal of Fish Diseases

    (1990)
  • A.L. Buschkiel

    Beiträge zur Kenntnis des Ichthyophthirius multifiliis Fouquet

    Archiv für Protistenkunde

    (1910)
  • A.L. Buschkiel

    Neue Beiträge zur Kenntnis des Ichthyophthirius multifiliis Fouquet

    Archives Néerlandaises de Zoologie

    (1936)
  • A.D. Butcher

    Observations on some phases of the life cycle of Ichthyophthirius multifiliis Fouquet, 1876, a ciliate protozoan parasite of fresh-water fish

    Australian Zoology

    (1943)
  • A.D. Butcher

    Ichthyophthiriasis in Australian trout hatchery

    The Progressive Fish-Culturist

    (1947)
  • K.D. Cain et al.

    Characterization of mucosal and systematic immune responses in rainbow trout (Oncorhynchus mykiss) using surface plasmon resonance

    Fish and Shellfish Immunology

    (2000)
  • M.F. Canella

    L’apparato vestibolo–bucco–faringeo di Ophryoglena

    Pubblicazione del Civico Museo di Storia Naturale di Ferraro

    (1964)
  • M.F. Canella et al.

    Contributions à la connaissance des Ciliés. VII Biologie des Ophryoglenina (Ciliés Hyménostomes Histophages). `L’époque des ultrastructures’ de la ciliatologie: pourra-t-elle aboutir à une systématique phylogénétique ou s’agit-il d’une flatteuse illusion?

    Annali Dell’Universita Di Ferrera, Seg.II Biologia Animale

    (1976)
  • G.B. Chapman

    Ultrastructural aspects of the host–parasite relationship in ichthyophthiriasis

    Transactions of the American Microscopical Society

    (1984)
  • G.B. Chapman et al.

    Ultrastructure aspects of the somatic cortex and contractile vacuole of the ciliate Ichthyophthirius multifiliis Fouquet

    Journal of Protozoology

    (1983)
  • Clark, T.G., Dickerson, H.W., Gratzek, J.B. and Findly, R.C., (1987). In vitro response of Ichthyophthirius multifiliis...
  • T.G. Clark et al.

    Developmental expression of surface antigen genes in the parasitic ciliate Ichthyophthirius multifiliis

    Proceedings of the National Academy of Sciences of the USA

    (1992)
  • Cited by (0)

    View full text