Plate 24 and Fig. 5 (pp. 155–156).
Known world-wide from fish of the families Cyprinidae, Poecilidae, Cichlidae and Centrarchidae. Records of African hosts, all from southern Africa (Transvaal), include common carp, Barbus kimberleyensis, B. trimaculatus (Brandt et al., 1981; Van As et al. 1981) and Oreochromis mossambicus (Van As, personal communication). Records of hosts from the Near East include, Common & Koi carp, Tor (=Barbus) canis, Mirogrex terrae sanctae, Tristramella spp. (Cichlidae), Gambussia affinis (Israel); common carp, Barbus spp. (Iraq, Khalifa, 1986).
The worms, originally described in Japan and China, were apparently already introduced populations, while the natural host and geographical origin of this tape worm is the grass carp (Ctenopharyngodon idella) of the Amur river. By 1954–1962, infections had become widespread in farmed fish (in European and Chinese carp) as well as in a variety of wild fish in both the Asian and European USSR (Bauer & Hoffman, 1976). By 1970–1975 records of infections came from Hungary, Yugoslavia, East and West Germany (Molnar & Murai, 1973; Korting, 1974; Bauer & Hoffman, 1976), and by 1980, worms had become prevalent in France (Denis et al., 1983), Britain (Andrews et al., 1981), South Africa (Van As, Schoobee & Brandt, 1981), USA, and Mexico. Worms were introduced into Mauritius via South Africa (Van As, pers. comm.). New records also came from Asia; Israel, Iraq (Khalifa, 1986), Malaysia (Fernando & Furtado, 1964), Sri Lanka (Fernando & Furtado, 1963) and Korea (Kim, et al., 1985).
Allied species: B. aegypticus, known only from Egypt (Amin, 1978), and B. kivuensis, which occurs in Central and South Africa (Baer & Fain, 1960; Mashego, 1982).
Taxonomy, description and diagnosis
Bothriocephalus acheilognathii was originally described as three different species, but these were later recognised as synonyms (Korting, 1975; Molnar, 1977), described from wild fish in Japan (as B. acheilognathii Yamaguti, 1934 and Bothriocephalus opsariichthydis Yamaguti, 1934) and from grass carp (Ctenopharyngodon idella) from South China (as B. gowkongensis Yeh, 1955).
Infection can be readily detected from faecal material, revealing eggs, or residues of segments, and by autopsy, with the recovery of tape worm segments and scolices from the gut contents.
Eggs are operculated, 46–48 × 32–34 μm (Korting, 1975), 50–52 × 33–37 μm (Molnar & Murai, 1973) 53–54 × 33–38 μm (Yeh, 1955) and premature when laid. Worms are variable in size and number of segments. The scolex is heart-shaped, laterally flat, usually with a distinct terminal disk and deep lateral grooves (bothridia). Mature segments are broader than long, while gravid segments are longer than broad. Each segment contains 50–90 testes, the cirrus is located immediately in front of the vagina, the cirrus sac is round and the genital atrium is situated in the median line of the dorsal surface of the segment. The ovary is comprised of two lateral lobes connected by an isthmus, and vitellaria, approximately 200, scattered laterally (Yeh, 1955).
Differential diagnosis: Holarctic species of Bothriocephalus have a characteristically elongated scolex. Heart-shaped scolices also occur in B. kivuensis (Baer & Fain, 1958) and B. aegypticus (Rysavy & Moravec, 1973), reported from African cyprinids (Barbus spp.). B. aegypticus, however, has 140–200 testes (140–280, Amin, 1978) and its eggs are 66 × 34–46 μm (Rysavy & Moravec, 1973) 38–66 × 26–46 μm (Amin, 1978). B. kivuensis has 50–75 testes and its eggs are 50–54 × 34–36 μm in size (Baer & Fain, 1958, 1960). B. kivuensis, however, seems to be a valid species as it has been described from L. Kivu prior to the spread of B. acheilognathii into Africa (1958). This may not be the case for the more recently reported and future findings of bothriocephalids in cyprinid fish from habitats where B. acheilognathii is already present (in South Africa, Mashego, 1982). Differentiation between the autochthonous and the introduced bothriocephalid from such regions may be extremely difficult by morphological criteria alone.
B. prudhoei, from Clarias anguillaris in Egypt, distinctly differs from the above by its elongate rather than heart-shaped scolex (Tadros, 1966).
Life history and ecology
The life history of B. acheilognathii involves a definitive host, a fish and an intermediate host, a copepod.
The Asian tape worm seems to be a thermophilic species (Hoffman, 1980). Low temperatures seem to delay or even interrupt development and consequently completion of the life cycle. At 28–30°C, 77% of the eggs hatched in the first day after release, the remainder during the following five days. At 14–15°C, the incubation period extended to 10–28 days and was for all practical purposes interrupted below 12°C.
The ubiquitous, cosmopolitan copepod, Mesocyclops leuckarti, is a frequent intermediate host of the Asian tapeworm, particularly in large bodies of water. Other genera of copepods, Thermocyclops, Ectocyclops and Paracyclops, found in fish ponds in China and Korea (Liao & Shih, 1956; Kim et al., 1985), and Cyclops abyssorum in Northern Germany (Korting, 1975), are also compatible intermediate hosts. Thermocyclops oblongatus, common in certain dam reservoirs in Transvaal, has been suggested as the intermediate host there (Van As et al., 1981). The copepod Acanthodiaptomus and cladocerans (Daphnia) have been found to be incompatible as hosts (Molnar, 1977).
In Mesocyclops leuckarti from Lake Kinneret fed on coracidia, the ciliated larvae hatched from eggs incubated for 24 hours at 24°C, up to 14 procercoids became established per copepod and developed into infective stages after 15 days at the same temperature. Kim et al. (1985) report completion of procercoid growth in the copepod 17 days after infection, at 25°C. Korting (1975) reports completion of development, at the same temperature, after 10 days. Liao and Shih (1956) report completion of development to the infective stage after five days at 20°C, four days at 25°C and 21 days at 14°C. Differences in the reported timing of development may be explained by the following: procercoids may become infective before they complete their growth, also, copepods of different genera and species may vary in their compatibility as intermediate hosts, and lastly, growth is apparently affected by the number of procercoids in the copepod (as suggested by Korting, 1975).
Procercoids develop into mature worms within 21–23 days at 28–29°C (Liao & Shih, 1956) and 1.5–2 months at 15–22°C (Davidov, 1978). In the spring-summer ambient conditions of Lake Kinneret (16–28°C) it has been extrapolated that worms require at least two months to reach the gravid stage.
Davidov (1978) found that temperatures below 15°C will delay development to 6–8 months and suggested a life span of two or more years for populations of worms infecting fish in cold water systems. The absence of adult worms in B. canis, in Lake Kinneret, by mid-summer may imply a life span of one year. This may be the rule for infections existing in fish in warm water environments. The life-span of the reduced-sized worms of small fish (see below) is apparently even shorter, as they disappear by the turn of the season from the on-growing fish.
Worms demonstrate exceptional versatility in accommodating their sizes, i.e., biomass, to their host size, usually irrespective of species. In young (about 100–150 mm in length) carp and grass carp mature tapeworms consisted of up to 500–600 segments, (Molnar & Murai, 1973). In T. canis longer than 60mm and cichlids longer than 40 mm from Lake Kinneret, mature worms consisted of at least 100 proglotids and gravid worms contained 150–350 and exceptionally up to 580 proglotids. Worms with the same range of proglotids were recovered from pond cultured, 50–61 mm long, Koi carp. In small fish, juvenile T. canis, <50 mm in length and cichlids, <35 mm in length and also in G. affinis, mature worms consisted of less than 60 proglotids and gravid worms of less than 100 proglotids. In very small fish, cichlid fry 17–20 mm in length and young G. affinis, mature and gravid worms contained less than 50 proglotids and even as few as 17–20.
Other African species of Bothriocephalus
B. kivuensis: Baer & Fain (1960) report (at 20–25°C ambient temperatures) hatching of eggs within 41hrs and 50% of coracidia survived 20hrs (maximum to 34hrs). A local (L. Kivu system) copepod, Ectocyclops rubescens, feeding on coracidia, yielded precercoids which completed development in 16–19 days, but attempts to infect tilapia by feeding them on these copepods failed.
B. aegypticus: Eggs completed development to coracidia in 24hrs at 24°C and in 6 days at 18–20°C. In Egypt, in the Nile, the copepod host is Mesocyclops leuckarti. Procercoids complete development in the copepods in 8–10 days (Rysavy & Moravec, 1973).
Heavily infected fish have a distended abdomen. Sometimes infected fish also develop a variable degree of aseptic dropsy.
Tapeworm-infected grass carp in China suffered from high mortalities (Yeh, 1955). Bauer, Musselius and Strelkov (1969) report high mortality among heavily infected juvenile carp (90%) and also report pathological changes in infected fish, which include pressure lesions, inflammation of the intestine and severe “catarrhal-haemorrhagic enteritis” at the parasite attachment point, with proliferation of the peripheral connective tissue. Hoffman (1980) reports that the intestines of infected small fish, such as the golden shiner, become plugged by the worms and in some instances are perforated. Minnow farmers report mortality among infected stocks. Granath and Esch (1984) state that survival of G. affinis is significantly reduced compared with uninfected fish. Laboratory experiments also demonstrated that mortality caused by tape worms was a function of parasite density and host size. At elevated temperatures (to 25 and 30°C) survival of both infected and non infected fish declined, but infected fish died sooner.
Scott and Grizzle (1979) found considerably less pronounced pathological changes in infected grass carp and golden shiner (Notemigonus crysoleucas). Lesions were restricted to the attachment site. They also found similar haematocrit and condition values in both infected and control fish.
Accurate evaluation of the pathological effects of infection should be related not only to worm burden, but also to the size and condition of the host. Although the Asian tape worm is not fastidious in the choice of host, it may have different degrees of compatibility with different host species, which may also be expressed as variation in tolerance and defence response among infected fish species.
In most introductions the actual route of entry was not identified, however, in most instances it was connected to the introduction of Chinese or European carp (Bauer & Hoffman, 1976; Brandt et al., 1981).
In warm water fish farms, as well as in temperate and cold regions, infections occurred primarily in the introduced carp species; European (Cyprinus carpio) and grass carp (Ctenopharyngodon idella) and also in pond reared ornamental carp (Koi). The tapeworm, once introduced, did not remain confined to farmed carp but also spread to native cyprinids and non cyprinid fish. Among the latter, Gambussia affinis, also a widely introduced species, became an important carrier of infection in both natural and man-made waters in the USA (Granath & Esch, 1983) and Mauritius (Van As, pers. comm.). In Southern Africa infection became highly prevalent in native Barbus spp. (Brandt, et al., 1981; Van As, Schoobee & Brandt 1981).
Infection may reach 30–156 mature and gravid worms per pond-reared carp 90–160 mm in length (Kim et al., 1985), and up to 20, although usually less than 10, in fully-grown grass carp (Scott & Grizzle, 1979). In large T. canis and cichlids, infection is rare (1–0.1%), but some of the infected fish harboured as many as 83 gravid worms. In juvenile T. canis, cichlids and Koi carp, the number of gravid worms is rarely higher than 10, averaging one to five. In cichlid fry (<25 mm in length) or in G. affinis, the number of mature worms rarely exceeds five. Granath & Esch (1983) report a worm burden of 2–33 in G. affinis, in a reservoir in North Carolina. Scolices (young, unsegmented worms) are far more numerous in all hosts, small or large, but only a few (<10%) apparently succeed in developing into adults.
Infections assume a clear seasonal pattern, with peak incidence in the summer or otherwise during spring and autumn, not only in temperate and cold climatic regions (Chubb, 1982) but also in the Mediterranean regions where ambient winter water temperatures rarely drop below 10°C (in Israel, in L. Kinneret and in South Africa). Infestation seems to become interrupted during the coldest part of the year as is evident from the complete absence of young scolices. The latter becoming predominant during the warmer part of the year. A study of G. affinis by Granath & Esch (1983) in southern USA showed, on the other hand, peak occurrences of early stage (“non segmented”) tape worms during periods of lower water temperatures.
Distribution and seasonality of Asian tapeworm infections depends not only on ambient temperatures but also on the abundance of compatible copepods, which is also seasonal, and their part in the composition of the fish's food, which is both age and season related.
The Asian tape worm in Lake Kinneret is sustained concurrently in three host communities; a perennial cycle in young of the year T. canis and seasonal (spring, summer) infections of inshore small fish including fry and fingerlings of cichlids and G. affinis. Infection is lost from the juvenile fish (T. canis and cichlids) as their diet changes from zooplankton to phytoplankton and detritus, to predation. The perennial nature of infection in the lake seems to be maintained by the sporadic infections which occur in T. canis older than the year. Prevalence of infection in juvenile T. canis is 35–50%, in fry of cichlids 25–40% and in G. affinis of all ages 50–99%.
Several chemotherapeutic formulations, when applied in food, effectively relieved fish from infection. Drugs should be mixed in oil (corn, soy, fish) and sprayed on to pellets or mixed with feeds at a rate of one litre per 70kg dry weight.
Di-n-butyl tin oxide: recommended dose, a total of 250 mg per kg of fish, fed over a period of 3 days (Mitchell & Hoffman, 1980).
Dibutyl tin dilurate (Tinostat): a poultry product, recommended to have better efficacy than the above tin formulation (Mitchell & Hoffman, 1980).
Yomesan (niclosamide, Lintex): 50 mg (active ingredient) per kg fish. Options for application are as follows: 500 g per 500 kg dry pellets fed at 1.5% of body weight, 2–3 times at weekly intervals; 28 g per 40 kg, fed for 3 days. A further option is the incorporation of either of the recommended doses into pellets and distributed over 7 feeding days at 5% of fish body mass (Korting, 1974; Mitchell & Hoffman, 1980; Brandt et al., 1981). Yomesan, however, is toxic to fish in aquaria and tanks without running water (Molnar, 1970; Hoffman, 1983).
Droncit (Praziquantel of Beyer) (experimental - Hoffman, G.L. personal communication): 5mg/kg of fish, by direct application or incorporated into pellets.
Eradication of infection will be more complete if combined with a control of copepods in the pond water. Recommended for use are insecticides employed as ectoparasiticides; Neguvon (Masoten, or Dipterex) or similar compounds (Bromex [Naled]).
Species affected and geographic range
A variety of adult stage tapeworms (over 40 species) occur in native African fish; monozoic (unsegmented) forms, notably Caryophyllaeidae as well as one amphilinid representative, and the segmented pseudophyllideans and Proteocephalidae (Khalil, 1971; Van As & Basson, 1984). Tapeworms are widespread throughout all major water systems of Africa and demonstrate a high degree of host specificity. Siluriform fish are the most common hosts for both monozoic and segmented cestodes. Caryophyllaeidae occur in a wider range of host families (Cyprinidae - Barbus spp., the characid Alestes nurse and in mormyrids). Common hosts of segmented tapeworms are also Polypterus spp. There is only a single record of tapeworms from cichlid fish - Proteocephalus bivitellatus (Woodland, 1937).
Life history and biology
Nesolecithus africanus, like other amphilinids occurs in the coelomatic cavity of its fish host, the mormyrid Gymnarchus niloticus (Donges & Harder, 1966). All other cestodes, monozoic and segmented, occur in the digestive tract. Wabuke-Bunoti (1980) reports entry of Polyonchobothrium clarias to its host Clarias mossambicus (= C. gariepinus) gall bladder.
Eggs of amphilinids apparently escape from the coelom through the genital opening and hatch only when ingested by an invertebrate intermediate host, such as amphipods in the case of sturgeon amphilinids (Bauer, 1959).
The first intermediate hosts of Caryophyllaeid cestodes are oligochaete worms, Tubifex and allied genera. Eggs, contained within, or released from evacuated dead worms are ingested and hatched within the digestive tract of the tubificid worm. The definitive host becomes infected when consuming infected oligochates (Bauer, 1959; Scholtz, 1991).
First intermediate hosts of segmented tapeworms; pseudophyllideans and proteocephalids are copepods. In Proteocephalus, a second larval stage, pleurocercoids, develops in fish species non compatible as definitive hosts (Hoffman, 1967).
Pathology and epizootiology
In naturally occurring infections, among fish in African aquatic habitats, damage to the host is rarely evident. These worms, however, pose a potential risk to native fish species introduced to farming (Clarias spp. and Heterotis niloticus). Wabuke-Bunoti (1980) reported some tissue response (inflammation) around bothria of P. clarias attached to gut mucosa in infected Lake Victoria C. gariepinus. In the same fish, however, bothridial penetration into the gall bladder mucosa causes pronounced nodules. Such nodules contained granulomatous and fibrous tissue. Entry of P. clarias to the gall bladder, however, was not observed in Clarias spp. infected by the same parasite elsewhere in Africa and the Near East (Paperna, 1964; Khalil, 1969, 1971).
Caryophyllideans infecting cultured European and Chinese carp (Caryophylleus, Khawia) were reported to cause, in heavily infected farmed fish, severe damage to the intestine (obstruction and enteritis) as well as upsetting the general condition of the fish (Bauer, 1959; Mitchell & Hoffman, 1980). However, these tapeworms have not, thus far, been found in exotic carp species farmed in tropical or southern Africa.
The same as for Bothriocephalus acheilognathii.
Species affected and geographic range
Infections with Ligula pleurocercoids in the body cavity and by encysted cyclophyllidean cysticercoids are widespread in Central and South African fish (Khalil, 1971; Mashego, 1982; Van As & Basson, 1984). Ligula infections are very common in Barbus spp. and in the open water cyprinid Rastrineobola (= Engraulicypris) argenteus of Lake Victoria. It also occurs occasionally in cichlids (Haplochromis spp. from L. Victoria, and Oreochromis sp. from Israel).
Cyclophyllidean cysticercoids are common and numerous in mesenteries of siluriforms, Clarias and Bagrus spp., and in cichlids; they have also been reported from Barbus spp.. Infections occur in the Sudan (Prudhoe & Hussey, 1977), in L. Victoria (Khalil & Thurston, 1973) and the lesser Rift Valley lakes, in L. Kariba, Zambia (Batra, 1984), the Niger (Ukoli, 1969) and in Ghana (Prah, 1969).
Taxonomy, description and diagnosis
Ligula pleurocercoids show very limited structural differentiation. They are flat, unsegmented and have a tapering anterior end with two bothridia. Pleurocercoids from different host fish vary in size, which ranges from 67–245 mm in length, and 3–10 mm in width. Ligula pleurocercoids collected from African fish were referred to as L. intestinalis (Prudhoe & Hussey, 1977; Mashego, 1982), a species widespread in European cyprinid fish which develops to the adult stage chiefly in gulls. In Africa, L. intestinalis has been reported from cormorants (Prudhoe & Hussey, 1977). It is, however, questionable whether Ligula from fish in Africa are conspecific with those from European fish, and if pleurocercoids found in different fish families are of the same species (Prudhoe & Hussey, 1977).
Cyclophyllidean cysticercoids are located in cysts up to 1 mm in size and are recognised by their hook-armed and sucker-bearing scolex. The cysticercoids were recognised as dilepidides, one species (encysting in Oreochromis niloticus), Paradilepis delachauxi, developed into the mature stage in a cormorant (Phalacrocorax africanus) (Prudhoe & Hussey, 1977). Cysticercoids from South African species of Barbus were assigned to the genus Parvitaenia (by Gibson, quoted in Mashego, 1982).
Life history and biology
First intermediate hosts of L. intestinalis are planktonic copepods which ingest the free swimming larvae (the coracidia hatched from the eggs). Procercoids develop to the stage infective to fish within 9–10 days in ambient European conditions, and will survive in the copepods for another 3–5 days (Bauer, 1959). Definitive hosts of L. intestinalis are various piscivorous birds. In the northern hemisphere, gulls are a very common hosts. African Ligula occurs in cormorants and L. intestinalis var. africana Joyeux & Baer, 1942 was described from Phalacrocorax africanus (Prudhoe & Hussey, 1977).
Eggs containing cyclophyllidean scolices were found in stomachs of very young cichlids in Lake Naivasha. Definitive hosts of these parasites are piscivorous birds, Paradilepis delachauxi, which as larvae infect Oreochromis niloticus, develop in the intestine of Phalacrocorax africanus (Prudhoe & Hussey, 1977).
Severe pathological changes were reported in infections of Ligula intestinalis in the northern hemisphere; fibrosis, inflammation and atrophy of the viscera, resulting from compression and displacement of the organs by the parasites, often together with accumulation of blood stained ascitic fluid (Bauer, 1959; Sweeting, 1977; Mitchell & Hoffman, 1980). Worms may comprise up to 10% of their host weight and exert pressure upon visceral organs and on the abdominal wall, but nonetheless, the effect on the host is variable, and such naturally infected fish often do not demonstrate a decline in condition. The more severely affected fish could, however, have escaped our attention by being eliminated through selective die-offs. Infected Barbus spp. in Southern Africa and R. argenteus in Lake Victoria are very noticeable due to the considerable distention of their abdomen, but evidently with no other clinical signs, except for diffuse haemorrhages in the abdominal wall in some fish. Infection in cichlids is not recognisable externally. In both Barbus and cichlids, only one Ligula pleurocercoid is usually recovered per individual fish and only exceptionally are 2–3 worms found in the abdomen of one fish. In R. argenteus, which exceptionally reaches an adult length of 80mm, it is not unusual to find two or even three, 40–60mm long, 5–7mm wide worms. Infection with L. intestinalis leads to interruption of reproductive functions (Sweeting, 1977). This, however, has not been examined critically in infections affecting fish in Africa.
Encysted cyclophyllaeid larvae usually occur in the mesenteries and as such do not interfere, even when numerous, with the physiological functions of the fish.
Data are too scanty and only available from wild fish. In some dam reservoirs in South Africa, prevalence of infection among certain species of Barbus (B. unitaeniatus) reaches 85% (Mashego, 1982). In some catches in Lake Victoria (in Kavirondo Gulf), over 70% of the R. argenteus were infected. Newly introduced Tinca tinca into fish ponds, in Israel, died out following infection with Ligula, however, precise details are lacking.
Heavy infections of encysted cyclophyllaeid larvae were found in large Clarias gariepinus and Bagrus docmac in Lake Victoria, and in Lake Naivasha in young Oreochromis spp., but there are no quantitative data.
Some chemotherapeutic agents used to treat adult stage cestode infections may be effective, in particular Droncit (see above). Mebendazole (5-benzoyi-1H-benzimidazol-2-vl) has been recommended specifically against migrating pleurocercoids (Mitchell & Hoffman, 1980). Treatment of ponds to eliminate copepods has also been recommended (see above).
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Plate 24. Tape worms (Cestoda): (page 155 with legend)
Fig. 5. (p. 156) Tape worms (Cestoda): Bothriocephalus aegypticus: A. egg (60×40 μm) (1), coracidium (60×70 μm) (2), onchosphere removed from (3) and inside the body cavity of Mesocyclops (4) and 7-day old procercoid (350×80 μm) from the Mesocyclops B. Scolex, C. mature proglotid (after Rysavy & Moravec, 1975). C. Polyonchobothrium polypteri Scolex (1), mature proglotid (2) and gravid proglotid (3). D. Amphilina, general view. E. Monobothrioides woodlandi (Caryophyllidae) (length 0.4mm) (after Makiewich & Beverly-Burton, 1967). F. Lytocestes marcuseni (Caryophyllidae) (length 0.6 mm) (After Troncy, 1977). H. Proteocephalus largoproglotis, scolex and mature proglotid (After Troncy, 1977). I. Dilepidid scolices from Oreochromis leucostictus, Lake Naivasha, free in gut (1) and still within egg shell in the stomach (2) (size: 1. scolex = 0.5×0.35 mm; 2. egg = 0.3 × 0.15 mm).
Plate 24. Tape worms (Cestoda): a. Scolex of Bothriocephalus acheilognathii from carp, Transvaal, South Africa (by courtesy of J.G. Van As). b. B. acheilognathii, whole worm (living) from farmed carp, Israel. c. Embryonated eggs of b. d. Ligula sp. from Rastrineobola argenteus from L. Victoria. Infected fish are recognised by their inflated abdomen (top fish) and may accommodate even three worms (bottom group).
Fig. 5. Tape worms (Cestoda) (legend p. 154).