Plates 25 and 26 (pp. 168 – 169) and Fig. 6 (p. 170).
Potentially all freshwater and brackish water fish may be affected, with heavier infections in predatory fish, particularly by species also utilising fish as intermediate or transient hosts.
Prevalent species are host specific and distributed as widely as their suitable hosts. Procamallanus laevionchus and Paracamallanus cyathopharynx are parasitic on Clarias (Khalil, 1969; Moravec, 1974a; Boomker, 1982) and also occur in the same host in the Near East (Paperna, 1964). An endemic species, Anguillicola (A. papernai Moravec & Taraschewski, 1988), occurs in the eels (Anguilla mossambica) of the Cape region of South Africa. The stomachs of Cape eels were also infected by the widespread Indo-Pacific eel parasite, Heliconema anguillae (syn. Ortleppina longissima) (Jubb, 1961), and elvers with Paraquimperia sp. (Jackson, 1978).
Taxonomy, description and diagnosis
Nematoda (round worms) are very distinctive in shape, with a solid cuticle. Because of their resistant cuticle these worms last longer than flatworms in post-mortem conditions. Most adult forms are large enough to be visible to the naked eye. Khalil (1971) reports 40 species of adult nematodes, representatives of 9 families from fish in Africa. The majority occur in the alimentary system and only a few enter tissues or inner cavities (Philometridae and Anguillicolla, the swimbladder).
Isolated nematodes should be fixed in warm (80–90°C) 10% neutral or saline formalin, or in 70% alcohol, and preserved in either solution, mixed with 1% glycerine. There are several morphological criteria which will allow recognition of representatives of most families and even some genera, and readers are referred to the relevant literature (CIH Keys for Nematode parasites of Vertebrates, Commonwealth Agricultural Bureaux: Fantham, UK - see Kabata, 1985; Essentials of Nematodology, edited by K.I. Skrjabin, published by the USSR Academy of Sciences, in part translated in to English [available from the US National Information Service]). Taxonomic determination, to genera and species, nonetheless needs wider experience in nematodology.
Life history and biology
Oxyuroidea (such as the Oxyuridae and Kathlanidae) are monoxenous (single host) and occur in the intestines of detritus feeders (Citharinus, Distichodus) and omnivorous fish (Synodontis, Oreochromis and Barbus - Khalil, 1971).
Copepods are first intermediate hosts to Camallanidae, Cucullanidae, Philometridae and Anguillicolidae. In Egypt, Moravec (1974b, 1975a) studied the life cycles of Procamallanus laevionchus and Paracamallanus cyathopharynx and obtained a development of the first three larval stages in Mesocyclops leuckarti. Camallanidae give birth to first stage larvae, which are ingested by the copepods. The larvae reach the third stage after two moults, P. cyathopharynx in 8–9 days at temperatures of 23–24°C (Moravec, 1974b).
Nematodes are often very fastidious in their choice of copepod hosts (and will not develop in species of Cyclops, Diaptomus or cladocerans). However, larvae of Anguillicola crassus developed successfully in an ostracod (Petter, Cassone & Le Belle, 1990). Ingested larvae pass from the gut into the copepod haemocoel. Longevity of such larvae in the copepods is variable (Thomas & Ollevier, 1993).
The first intermediate hosts of Rhabdochona and Spinitectus are aquatic larvae of insects (Mayflies, Gustafson, 1939; Hoffman, 1967). Eggs of some species of Rhabdochona are provided with filaments and some also have a gelatinous polar cap (Moravec, 1975b).
Larvae in copepods, or other invertebrate intermediate hosts, will develop to fourth stage larvae and further into adult males and females when ingested by a suitable definitive host (Moravec, 1974b). Larvae ingested by “wrong” piscine hosts often survive as waiting stages (fourth stage larvae) in the gut or other tissues for a variable length of time and continue development into the adult stage if their carrier host (parataenic host) is predated by the compatible host. This has been demonstrated in Procamallanus laevionchus (Moravec, 1975a), in the anisakids (Heterocheilidae) Dujardinascaris and Rhapidascaroides, and in species of Anguillicola (Petter, Fontaine & Le Belle, 1989).
Capillariid larvae often develop in oligochaetes (tubificids) and may also be transmitted via a parataenic piscine host. Such larvae may be found in visceral organs such as the liver (Moravec, Ergens & Repova, 1984). Larvae of some species (Capillaria pterophylli) infecting several South American cichlids will, however, reach their definitive hosts without an intermediate (Moravec, 1983). One genus, Schulmanela, thus far unknown in African fish, parasitises the liver and deposits its eggs there, which are only released after the host's death or predation (Moravec, Prokopic & Shlikas, 1987).
Philometridae occur in body cavities or penetrate subcutaneous tissues. Males, are short-lived and the ovoviviparous females extrude their posterior end through the skin to release larvae into the water. Fish become infected by ingesting infected copepods (Molnar, 1966; Paperna & Zwerner, 1976). The family Philometridae is represented in Africa by two genera: Nilonema gymnarchi in the lung-like air bladder sacs of Gymnarchus niloticus and Thwaitia bagri, under the skin lateral to the mouth in Bagrus bayad (Khalil, 1969). Gravid N. gymnarchi presumably escape from the lungs into the water to discharge larvae (Khalil, 1969). Gravid worms of T. bagri only appear during December–February. Strict seasonality reported in some species of Philometra was linked with the host reproductive season (Paperna & Zwerner, 1976).
Host specificity of nematodes is variable. Among the Camallanidae Procamallanus laevionchus has, thus far, been reported from fish hosts of six different families, while Spirocamallanus spiralis has only been reported from species of Clarias and Synodontis, Paracamallanus cyathopharynx only from species of Clarias, and Camallanus kirandensis only from a Barbus sp. Similarly Rhabdochona congolensis and Spinitectus allaeri have been reported from numerous diverse host species, while the other known species of the same genera occur in one or a few hosts, usually related species. Very host specific are species of Capillaria, most oxyurids and the philometrids Nilonema gymnarchi and Thwaitia bagri (see Khalil, 1969, 1971; Moravec, 1974a). Species of Anguillicola will only infect species of Anguilla (Moravec & Taraschewski, 1988).
Pathology and epizootiology
Infections by camallanids (Paracamallanus cyathopharynx and Procamallanus laevionchus) are abundant and heavy (up to 20 or more) particularly in the stomach of Clarias spp,. and in many other catfish. Spirocamallanus spiralis are also common in the stomach of the latter (Paperna, 1964; Khalil, 1969; Mashego & Saayman, 1980; Boomker, 1982). None of these were reported as pathogenic, in spite of the firm attachment by their buccal capsule to the stomach mucosa. Little harm is also caused by species of Rhabdochona or Spinitectus, common in the intestines of fish of all families (Paperna, 1964; Khalil, 1971).
Massive infections by Capillaria (Pseudocapillaria) and Capillostrongyloides which attach to and feed on the intestinal mucosa, caused emaciation and mortalities in aquarium reared neotropical cichlids and siluroids (Moravec & Gut, 1982; Moravec, Gelnar & Rehulka, 1987). Another species, C. brevispicula, which is widespread in European cyprinids and which caused the death of aquarium held tropical asian cyprinids (Moravec, Ergens & Repova, 1984) has also been introduced to carp reared in warm water ponds in Israel, but as yet, with no pathological implications. A massive infection by the cosmocercid nematode Railletnema synodontis has been reported from aquarium held Synodontis eupterus of African origin. These oxyurids feed only on the gut contents. Nonetheless, fish were in poor condition (emaciated) and their digestive tract exhibited signs of atrophy (Moravec & Rehulka, 1987).
Several species of Philometra and related filaroids cause mild to severe pathology in fish. Aged and dying worms locked in the abdomen or trapped in tissue provoke severe inflammatory responses, granuloma and fibrosis (Paperna & Zwerner, 1976). Infection with N. gymnarchi in the lungs and T. bargi in the vicinity of the mouth cause only light local tissue reaction (Khalil, 1969).
Five species of Anguillicola occur in eels native to Japan/China, Australia, New Zealand and South Africa, two (from Japan/China and New Zealand) were recently introduced into Europe apparently with elvers imported as culture seed (Moravec & Taraschewski, 1988). Infection is widespread in wild eels (Peters & Hartman, 1986) and occasionally occurs in earth ponds, but it is unlikely to spread in hyperintensive systems where copepods, the intermediate hosts, cannot usually survive (Hirose et al., 1976). Pathological effects vary with growth conditions and eel species. Heavy infection causes haemorrhagic inflammation of the swim bladder, but it may not necessarily always disrupt fish growth. It may, however, decrease the eels tolerance to transport stresses (Paggi et al., 1982). In South Africa, infection by an endemic species was found in cultivated eels only.
Experimental treatment of Anguillicola crassus in european eels by helminthicides (levamizol, mebendazol, or ivermectin) has produced satisfactory results. Levamizol was most effective, applied as a bath of 1 mg/l for 24hrs, when LD 50 to 20–40 cm eels was 250 mg/l for 24hrs (Taraschewski et al., 1988). Experience with other nematodes is lacking.
Potentially in all fresh and brackish water fish, with heavier infections occurring in fish occupying higher positions in the food-chain, e.g. predatory fish.
Contracaecum occurs in Israel (Paperna, 1964), Egypt, Mali, most large and small East African (Rift Valley) lakes (including lakes Kivu, Edward and Albert—Campana-Rouget, 1961), Zaire, Mali (Niger) (Khalil, 1971) and South Africa, where it was also reported from brackish water hosts (Boomker, 1982; Van As & Basson, 1983). Infections of the pericardia in cichlid fish occur in Israel (Landsberg, 1988) and in lakes Victoria, George, Nakuru, Naivasha, Baringo and Magadi (Paperna, 1974a; Malvestuto & Ogambo Ongoma, 1978). Amplicaecum was reported from the Sudan (Khalil, 1969) and Dujardinascaris from Lakes Chad and Tanganyika. Eustrongylides has, thus far, only been found in the East African Lakes, including L. Tanganyika (Campana-Rouget, 1961, Khalil, 1971; Paperna, 1974b).
Taxonomy, description and diagnosis
Most notorious larval nematodes are representatives of the Anisakidae (Heterocheilidae); genera Amplicaecum, Contracaecum and Porrocaecum, Dioctophymidae; the genus Eustrongylides and Rhabdochonidae; the genera Rhabdochona and Spinitectus, the latter two genera also infect fish at an adult stage and are discussed above (15.1).
Larval nematodes occur either encysted in tissues or free in body cavities, most often in the abdominal or pericardial cavity. Larvae of Contracaecum and Eustrongylides tend to escape from their cysts, and crawl out of their host body after its death. Larvae will usually emerge from isolated cysts if incubated in 0.9% saline solution at 37°C. Released worms can be examined live or after fixation in hot 4% formalin or 70% ethyl alcohol and cleared in glycerin or lactophenol.
Identification of larval nematodes, particularly to species level is not usually feasible, since the larvae lack genital systems and several other features of adult stages which are utilised as taxonomic criteria. In recent years a methodology of identification of larval stages (of Anisakidae) by biochemical (isoenzyme) methodology utilising multilocus electrophoresis analysis has been developed (Orecchia et al., 1986).
Rhabdochona and Spinitectus are very small (<10 mm in length), the former shows dentation in its mouth opening, while the cuticle of the latter bears circular rows of spines. Eustrongylides are large long red worms, 18–70 mm long, 0.3–0.8 mm thick, with a long oesophagus merging with an indistinct ventriculum (Paperna, 1974).
Anisakiid larvae are variable in size, often very large and thick, up to 60 mm long and 3 mm in diameter, with characteristic outgrowths (appendices) of either the anterior end of the intestine or the posterior end of the oesophagus (the vetriculum) or both: in Contracaecum appendices are formed (in opposite directions) from both the ventriculum and the intestine, while Porrocaecum has only one appendix of the intestine present and the ventriculum is separated from the oesophagus. Amplicaecum, differs from the latter, lacking a ventriculum distinctly separated from the oesophagus and in Dujardinascaris an intestinal appendix is present as well as a muscular ventriculum.
Life history and biology
Definitive hosts of Contracaecum are pelicans, cormorants and herons. Pelicans (Pelecanus onocrotalus), incriminated as the definitive hosts of Contracaecum (found in the pericardial cavity of farmed tilapia, Oreochromis hybrids), were found to be infected by two species, C. multipapillatum and C. micropapillatum, but only the former appears to be implicated in infections of tilapia (L. Paggi and colleagues, unpublished).
Eggs are released via defaecation. They are also released into water when whole nematodes are vomited from the stomach by regurgitation. Eggs are released from such discharged nematodes by oviposition or after death, following their decomposition. Eggs hatch within 2–3 days at 24°C, 5–7 days at 21°C; hatching is not simultaneous and is further delayed in some of the eggs. Free living infective (second) stage larvae can survive in water for several months. Larvae become firmly attached by their posterior end to a substrate in the aquatic habitat. Small crustaceans are the first intermediate hosts of anisakiid nematodes.
In Israeli fish ponds, copepods of the genus Cyclops were the first intermediate hosts to C. multipapillatum and C. micropapillatum obtained from pelicans and to C. rudolphi released from cormorants (Phalacrocorax carbo). Consumed larvae entered the haemocoel of the copepods while transforming into a subsequent developmental stage. Infection was retained in copepods for over 40 days. In those fish which became infected after consuming the infected copepods, larvae (third stage) migrated into the viscera, entered the swimbladder and finally accumulated in the pericardium (Landsberg, 1989; Paperna, unpublished). Within 2–4 months worms grew from 0.5 mm to 60 mm. They then persisted in the pericardium for up to 15 months (Landsberg, 1988), or throughout the second year after infection.
In South Africa, where encysted Contracaecum are common in a wide variety of fish of diverse families (Boomker, 1982; Mashego, 1982; Mashego & Saayman, 1980; Van As & Basson, 1984), C. micropapillatum, C. microcephalum and C. spiculigerum are found in cormorants and pelicans, and the latter also in herons (Prudoe & Hussey, 1977). Cormorants (P. africanus) also harboured C. carlislei (Boomker, 1982).
The life histories of other anisakiid worms are unknown except that Nile monitors (Varanus niloticus), water snakes, crocodiles, frogs and toads are definitive hosts of Amplicaecum and crocodiles are also hosts for some Porrocaecum and Dujardinascaris. Definitive hosts of other species of the latter genus are fish (Malapterurus electricus and Gymnarchus niloticus).
The first intermediate hosts of Eustrongylides are unknown, although oligochaetes are the first intermediate hosts of a related dioctophymatoid from the genus Hystrichia. However, the latter do not develop via fish. In fish, larval infection passes from prey (cichlid fish, mainly Haplochromis) to predator, finally accumulating in the predatory catfish, Bagrus docmac and Clarias gariepinus (=mossambicus) and also in the lung fish (Protopterus aethiopicus). Numerous adult Eustrongylides sp. were found attached to the stomachs of cormorants (Phalacrocorax africanus) obtained from the same habitats (in Entebbe, L. Victoria) where fish were heavily infected (Paperna, 1974b). Herons, snakebirds (Anhinga rufa) and pelicans in the Sudan are hosts to Eustrongylides africanus (Jagerskiold, 1909).
Neither encysted nor free Contracaecum larvae will severely affect fish. Tissue reaction, inflammation, epitheloid formation and fibrous encapsulation around encysted larvae is localised. Multiple infection of the mesenteries resulting in extensive inflammation, fibrosis and even some visceral adhesions, were seen only in large fish, with no apparent impact on their body condition (Mbahinzireki, 1980). Worms inhabiting the pericardial cavity do not induce any visible damage. Large (200–350 g) tilapia can accommodate up to 12 worms, which may reach a length of 6 cm and 2–3 mm in diameter. However, these infections, which affect the large fisheries of L. Naivasha in Kenya and intensive tilapia pond cultures in Israel, cause significant loss of income to these enterprises. As worms tend to migrate to the surface once fish die, such “wormy” fish deter customers. Fish have to be de-gutted and fileted in order to be sold for consumption, the cost of which has to be paid by the producers.
There are no indications of pathological effects caused by Amplicaecum larvae inhabiting the sinus venosus of cichlids or the body cavity of siluroids and other fish (Khalil, 1969).
Eustrongylides larvae in cichlids, when unencysted, migrate under the skin and in the muscle causing extensive inflammation and necrosis. Encysted worms in the visceraliver, spleen and the gonads - cause severe pathological changes in the adjoining tissue. In the spleen, the tissue is replaced by lipid cells. Infection in the testes or ovaries causes severe pressure necrosis, degeneration of the spermatogenous and follicular tissue, being either replaced by lipid cells or undergoing complete necrosis, ultimately resulting in castration. The incidence and the degree of damage to the gonads was positively correlated with the overall burden of infection in the fish. In large catfish and lungfish, larvae are numerous (often over 100) but they encyst only in mesenteries. Even heavy infection induces localised inflammatory response, while essential visceral organs are unaffected. One heavily infected B. docmac was emaciated, but otherwise fish condition (determined using weight/length indices) did not seem to be affected (Paperna, 1974b).
Epizootiology of the pericardium inhabiting Contracaecum is linked with migration of piscivorous birds, particularly (or even only) pelicans, between Europe and tropical East Africa. Infection of ponds in Israel occurs after they have been visited by pelicans during spring migration. Definitive hosts of the other forms of Contracaecum (piscivorous birds), Amplicaecum (aquatic reptiles) or Eustrongylides (cormorants), are apparently sedentary as infection is geographically localised.
Prevalence of pericardial Contracaecum infection among tilapia in a contaminated pond often approaches 100%, usually with 1–4 worms per fish. In Lake Naivasha, Kenya, 85% of Tilapia leucosticta were reported infected with a mean of 9 worms per fish, in L. Baringo 70% of O. niloticus with 5 worms per fish, in L. Magadi 30% of T. grahami with a mean of 2 worms per fish and in Lake George 30% of (270 mm long) O. niloticus with a mean of 1 worm per fish (Paperna, 1974b; Malvestuto & Ogambo Ongoma, 1978). Pericardial Contracaecum has not yet been seen in the numerous cichlids inspected in South Africa.
Among cichlid fish in the Sudan Nile, 94% of Oreochromis niloticus, 82% of Sarotherodon galilaeus and 69% of Tilapia zillii were reported to have Amplicaecum larvae in the sinus venosus, at 2–8 worms per fish. Amplicaecum also occurred in the body cavity of various predatory fishes at prevalence levels of 10–37% with worm burdens of up to 36 per fish (Khalil, 1969).
Eustrongylides larvae, if ingested by another fish, will re-encyst in its new host, this causes larvae to accumulate in predators at higher trophic levels. These, usually large catfish and lungfish, are beyond the reach of cormorants and are therefore, a dead-end for the parasites' transmission cycle. Accumulation of nematode larvae in the large predator fish may have considerable ecological importance in moderating parasite populations in lake fish. Among Haplochromis spp. of northern Lake Victoria, incidence of infection ranged from 17 to 52% (mean 27%) with a mean worm burden of 5.1 (SD=9.3) and up to 17 per fish. A quantitative study of B. docmac from the same fishing area in the lake revealed a 77% prevalence of infection, with a mean burden of 26 (SD=29-overdispersed) and up to 125 worms per fish (Paperna, 1974b). Similar data were obtained in a later survey by Mbahinzireki (1980).
Castration, resulting from invasion of the gonads, with a prevalence of infection ranging from 5 to 17%, was found in 6 out of 15 representatives of Haplochromis and Haplochromis related species from L. Victoria. Incidences of castration were more abundant in species demonstrating an overall higher prevalence of infection. Although Eustrongylides infections occurred in Haplochromis from L. George in none of these were the gonads involved (Paperna, 1974b).
Prevention of larval nematode infection by keeping away piscivorous birds is impractical not only in fishing areas in natural habitats or man-made impoundments but even in fish ponds. In fish ponds preventive treatments of Contracaecum by elimination of copepods (by insecticides such as Masoten or Bromex - see previous chapter on Cestoda) may be of some value if suitably timed, soon after its contamination by pelicans. Bromex, applied at a level of 2 ppm, killed free living larvae in vitro, but such a dose is about, or beyond, the tolerance limit of fish. Experiments with helminthicides (levamizol, mebendazol, or ivermectin) have not so far produced satisfactory results (I. Bejerano, pers. comm.) and it is not certain if costs of treatment (by use of medicated feeds) will be economical for tilapia farming.
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Van As, J.G. & Basson, L. 1984. Checklist of freshwater fish parasites from southern Africa. S. Afr. J. Wildl., 14: 49–61.
Plate 25. Nematoda: a. Juvenile (L5) of Procamallanus laevionchus, intestine of Clarias gariepinus, S. Africa. b. Anguillicola papernai in swimbladder of Anguilla mossambica, S. Africa. c. Contracaecum larvae in the pericard of pond Oreochromis aureus x niloticus, Israel. d. Egg of Contracaecum micropapillatum from Pelecanus onocrotalus, 3 days old. e. Free stage C. micropapillatum larva (L2). f. C. micropapillatum larvae in a copepod. g. Contracaecum larvae in viscera of Eutropius depressirostris, S. Africa (Transvaal).
Plate 26. Nematoda continued; Leeches: a–k. Eustrongylides larvae in fish in L. Victoria: a, escape of larvae from a dead haplochromid fish; b, encapsulated and freed larvae on the gut wall of Bagrus docmac; c. Larval nodules in spleen of a haplochromid; d. nodules in testis, and e,f, in ovaries of haplochromids; g. atrophic infected ovary in a haplochromid; h, lesions (L, arrows) due to migrating larvae in muscles of a haplochromid; i, lesion (L) with infiltration of lipid cells (F) in the spleen; k. fibrous lesion (L) in the ovary (o- oocyt). I Piscicolid leeches on the roof of the mouth of Liza tricuspidata, S. Africa, arrows: haemorrhages.
Fig.6. Nematoda: A. Rhabdochona congolensis, anterior and posterior ends (length -males 6–8 mm., females 16–21 mm.) B. Spinitectus allaeri, anterior and posterior ends (length - males 3–5 mm, females 4–7 mm). C. Procamallanus laevionchus, anterior and posterior ends (length - males 5 mm, females 4–5 mm.). D. Cucullanus barbi, male anterior and posterior ends (length - males 10–13 mm., females 4–7 mm.). E. Paracamallanus cyathopharynx mouth capsule. F. Spirocammallanus spiralis mouth capsule. G–J. Position of ventricular (g) and intestinal (i) coecca in larval Heterocheilidae: G. Amplicaecum, H. Porrocaecum, I. Contracaecum, J. Dujardinascaris with muscular ventriculus (m). o, oesophagus. (A – D, after Moravec, 1974a.)
Plate 25. Nematoda (legend p. 167).
Plate 26. Nematoda continued; Leeches (legend p. 167).
Fig. 6. Nematoda (legend p. 167).