Plates 20 & 21 (pp. 118 & 119) and Figs. 3a & 3b (pp. 120 & 121).
Fresh water and brackish water fish from most families of Teleostei (Khalil, 1971; Paperna, 1979).
Present in all inland waters of Africa. Species, and often also genera, of Monogenea demonstrate a high degree of host specificity, and follow their respective specific fish hosts throughout their distribution range. African species of Monogenea of Clarias spp. and of Cichlidae occur on hosts from the same families present in the Near East. Cichlid monogeneans, including the endoparasitic Enterogyrus cichlidarum (of Oreochromis niloticus and O. mossambicus), were introduced with their hosts to Southeast Asia (Natividad et al., 1986; Bondad-Reantaso & Arthur, 1990). On the other hand, exotic monogeneans were introduced with their specific hosts into Africa; Dactylogyrus minutus, D. anchoratus and Pseudoacolpenteron pavlovskii with carp (Paperna, 1980) and Acolpenteron ureteroecetes with the American large mouth bass Micropterus salmoides (Du Plessis, 1948).
Taxonomy, description and diagnosis
Monogeneans are flatworms (Platyhelminthes), ectoparasitic and attached by special posteriorly positioned attachment organs to their host's skin or gills. Their anterior end contains apical sensory structures, a mouth with or without accessory suckers and special glands or clamps for attachment. All are hermaphrodite. The testis is single or follicular; sperm are evacuated into a specialized, often sclerotinized copulatory organ. Female organs include ovary and follicular vitelline glands. The uterus usually contains no more than one, or only a few eggs. The South American oviparous gyrodactylids may have up to 20 intra-uterine eggs. One group, the Gyrodactylidae are viviparous; the uterus contains prenatal offspring and vitelline follicles are lacking.
Mongeneans are subdivided into several major taxa; Dactylogyroidea, Caspaloidea and Polyopisthocotylea. Most monogeneans found in inland water fish are Dactylogyroidea. Monogeneans of the latter two taxa are usually larger in size and are predominantly parasites of marine fish. Polyopistocotylea from three genera (two families) occur in African freshwater fish.
Dactylogyroidea are 0.3–2 mm long and usually have one or two anterior-dorsal pairs of eyes and a posterior-ventral attachment organ (the opisthaptor). This disk-like organ contains centrally positioned sclerotinoid anchors, connected to support bars and marginally located hooklets. Most dactylogyroids are gill parasites, only a few are skin parasites, most notably Gyrodactylidae. A few are specialised endoparasites inhabiting the nasal cavity (Paraquadriacanthus - Ergens, 1988a), the stomach (Enterogyrus -Paperna, 1963c) and the ureter (Acolpenteron - Du Plessis, 1948).
Diplozoidae and the diclidophoric Heterobothrium fluviatilis (Euzet & Birgi, 1975) like other Polyopisthocotylea have developed secondary clamps and hooks to replace the primary dactylogyroid opisthaptor. They lack eyes and their mouth is supported by a pair of suckers. A special characteristic of Diplozoidae is the permanent attachment for copulation of pairs of mature worms (Bykhowski, 1957).
Taxonomic subdivision of the Dactylogyroidea is based on structural variation in the sclerotinoid attachment organs in the opisthaptor (for the generic division) and of the sclerotinoid copulatory organ (for specific differentiation). Specific differentiation of monogeneans other than Dactylogyridae requires consideration of a wider range of morphological and anatomical characters (Bykhowski, 1957; Paperna, 1979).
Lower taxa of Dactylogyroidea can be differentiated as follows:
Gyrodactylidae: Viviparous, eyes absent, parent worm contains a distinct well differentiated embryo. Vitellaria not distinct, one pair of anchors, firmly attached by two bars. Gyrodactylus is the type genus. Species from the other genus, Macrogyrodactylus, are larger and carry additional sclerites in the anchor-bar complex.
All remaining Dactylogyroidea are oviparous with prominent vitelline follicles, usually with one to two pairs of pigmented eyes, the anchor only loosely connected (through ligaments) with the bars.
Diplectanidae: Anchors, two pairs, associated with three bars and ventral and dorsal concentric platelets (the squamodiscs).
Diplectanum lacustris in gills of Lates spp. (Thurston & Paperna, 1969). The parasite population was comprised of slender (0.6–1.0 × 0.15–0.25 mm) and gravid (1.0–2.0 × 0.3–0.5 mm) worms (Paperna, 1979). Slender and gravid forms of Diplectanum in Dicentrarchus punctatus were separated into two distinct species (Lambert & Maillard, 1974).
Dactylogyridae: Squamodiscs absent.
Pseudoacolpenteron and Acolpenteron have only marginal hooklets, the first is a gill ectoparasite of carp and has eyes. The second is an endoparasite of the urinary system.
The genera Dactylogyrus and Dogielus, parasitic in cyprinids, have one pair of anchors.
Members of genera characterised by two pairs of anchors (similar or dissimilar in size) and a variable number of bars (Ancyrocephalinae) occur in a variety of African fish families (Paperna, 1979; Ergens, 1981, 1988a, 1988b; Kritsky et al., 1987; Kritsky & Kulo, 1988, 1992; Douellou, 1993).
A variety of species found in hosts of diverse fish families have been assigned to Ancyrocephalus, but in fact are representatives of diverse (still undefined) generic entities. Cichlidogyrus, Onchobdella (with one species adapted to infect the skin - Paperna, 1968) and Enterogyrus (endoparasitic in the stomach) are host specific to diverse cichlid fish species. The genera Annulotrema and Characidotrema are host specific to characid fish. Afrocleidodiscus occurs in both Characidae and Citharinidae and fish of the latter family are also hosts for Nanotrema. Several genera occur in siluriforms, some are congeneric (Quadriacanthus) and others have a definite affiliation to dactylogyroids infecting Southeast Asian siluroids (Ha Ky, 1968; Paperna, 1979).
Dactylogyridae which have partly or completely lost one of their four anchors (Heterochocleidinae) parasitise gills of Ophiocephalus (Eutrianchoratus) and Ctenopoma (Heteronchocleidus) (Paperna, 1969; Euzet & Dossou, 1975), and are affiliated to dactylogyrids infecting fish of the same families (Ophiocephalidae and Anabantidae) in Southeast Asia (Lim, 1986, 1989).
Diplozoidae of two genera occur in African fish; Diplozoon (D. ghanense in Alestes spp. and D. aegyptienses in various cyprinids) and Neodiplozoon (two spp. in Barbus spp.) these being differentiated by the number and arrangement of the clamps (Paperna, 1979). The other polyopistocotylid, Heterobothrium fluviatilis occurs on Tetraodon fahaka (Euzet & Birgi, 1975).
For differential diagnosis, worms should be removed from the gills or the skin. This must be performed on freshly killed fish. Gills should be removed without excessive haemorrhaging and before becoming covered by copious mucus. Mucus production is prevented and worms are readily collected from gills after a few hours immersion in 1–2% formalin. For microscopic study of the sclerotinoid organs, required for differential diagnosis of Dactylogyroidea, worms are either embedded after fixation in 4% formalin, under pressure in glycerin jelly, or fixed and embedded in ammonium-picrate-glycerin. Both preparations are suitable only for temporary storage (6 months–1 year). For the larger non-dactylogyroid monogeneans (for example Diplozoon), fixation and staining methodology for tapeworms and trematodes should be applied.
Life history and biology
All monogeneans except gyrodactylids are oviparous. The uterus contains only very few eggs, often only one, but overall daily production may range from 5 up to 60. Egg production varies with age of the worm. Adverse living conditions (due to water quality or host responses) often accelerate oviposition (Izumova, 1958) and eggs are deposited undeveloped. All eggs except those of dactylogyroids have a long filament which helps the egg to remain tied to the gill basket or to a substrate in the water. The filament in the dactylogyrid egg is rudimentary and development of the egg to hatching takes place on the bottom of the aquatic habitat (Bykhowskii, 1957; Paperna, 1963a; Imada & Muroga, 1978).
Incubation time is temperature dependent. Eggs of Dactylogyrus species from carp hatch within two to six days at temperatures of 20–28°C. Embryonic development is enhanced and hatching is stimulated in the presence of fish mucus (Shaharom-Harrison, 1986). Emerging larvae (onchomiracidia) are free swimming, covered by tufts of cilia, bear two pairs of large pigmented eyes and already have a distinct opisthaptor with developed marginal hooks (hooklets) and primordia of anchors. The life span of the free swimming larvae at 20–28°C is 12–48h, but after 4–6 hours larvae apparently loose their ability to reach their hosts (Izumova, 1956; Bauer, 1959; Paperna, 1963a; Prost, 1963). Larvae are either actively attached to the skin of the host fish and then migrate to the gills or become attached when washed with swallowed water through the gills (Paperna, 1963a,b).
In dactylogyroids, development to maturity is usually fast (4–5 days) and life span is short, 5–40 days (Paperna, 1963a, 1963b; Shaharom-Harrison, 1986). Development of Diplozoidae to maturity and to the formation of copulating couples is slower, while the life-span of the adult worm is extended from several months to two years. Diplozoon paradoxum infecting European fish reach maturity only after 4 months, the life-span extending to two years and with reproductive activity restricted to the warmer part of the year (Bychowski, 1957; Bovet, 1967). Prolonged life span (over a year) with reproduction limited to the warmer part of the year (although intrauterine eggs were seen also in winter) has been observed in D. minutus infecting small cyprinids of the genera Tylognatus and Phoxinellus in Lake Kinneret, Israel (Paperna, 1963d, 1964a,b). Species found on tropical fish may have a considerably shorter development, of one to a few weeks and a life span of less than a year (Stebra, 1957). In Diplozoids (of the genera Diplozoon as well as Neodiplozoon), pairs of clamps appear gradually as the larvae differentiate, development is asymmetric and developing worms may show unpaired numbers of clamps (Paperna, 1963d, 1979). D. minutus juveniles join into couples before they reach maturity, at stages ranging from one pair to several pairs (or unpaired) clamps. Couples may be comprised of worms at different stages of differentiation as evident from a disparity in the number of clamps between the coupling worms. Larval stages were found to be less fastidious in their choice of host and natural as well as experimental hosts include other genera of cyprinids, juvenile carp and Oreochromis spp., but formed couples only on their specific hosts (Paperna, 1963d).
The Gyrodactylidae are viviparous. Worms give birth to fully developed adults. Intra-uterine embryos already contain second and often third generation embryos, recognised by their developing marginal hooklets and anchors. The life cycle of Gyrodactylus bullatardis on Lebistes reticulatus, from egg to egg at an ambient temperature of 25–27°C, is completed within 54–60 hours; new specimens first give birth, followed by each subsequent birth, after 18 hours. Eggs develop into embryos ready to be born within 36 to 42 hours (Thurnbull, 1956; Bykhowskii, 1957). The succession of embryos is formed through a process of polyembryony. The new born worm gives birth at least twice before it is inseminated and its own egg becomes fertilised. One of the blastomeres formed in the very early cleavages, separates and later becomes the origin of the following generations. Each fertilised egg gives rise to two subsequent series of embryo successions. In the new born worm male genitalia are still rudimentary, and become functional in older specimens when female reproduction ceases. Passage from host to host requires a direct physical contact between the fish (Thurnbull, 1956; Hoffman & Putz, 1964; for detailed description of the reproductive development of Macrogyrodactylus polypteri see Khalil, 1970).
Fish appear to co-exist with their specific monogeneans, in natural habitats as well as in culture conditions, even when infestations are intense. A few monogeneans, notoriously gyrodactylids, are, however, pathogenic to their host fish, usually to younger fish and in intensive culture conditions. Histopathological changes in the gills, are hardly detectable in most instances even in relatively intense infections. In Lates albertianus, intense hyperplasia developed around Diplectanus lacustris attached to gills; diplectanid infections are nonetheless pathogenic to cultured marine fishes (Oliver, 1977; Paperna, 1991).
D. vastator infection, in the gills of carp fry, induces severe hyperplasia of the gill filament epithelium. Extreme proliferation of the respiratory epithelium of the gills interferes with respiratory function and seems to be the cause of death (Paperna, 1963b, 1964c). D. lamellatus, in grass carp, induces epithelial proliferation, but also wounds the gill filaments where it is attached (Molnar, 1972). The largest among carp dactylogyrids, D. extensus, causes only focal cellular damage at its attachment site at the filament base. However, infections by this parasite were nonetheless, at times, fatal to both young and fully grown fish (Bauer, 1959; Prost, 1963; Sarig, 1971). In carp fry, D. vastator loses its attachment once the entire gill filament is taken by hyperplasia. Worm populations decline from 50–130 to 0–25 per fish at the height of the proliferation process. Recovery of the gill integument in surviving fish results in reinfection and consequently renewal of the proliferation process. D. vastator preferentially settles at the extremities of the gill filament. With the elongation of the gill filaments in growing fingerlings, the parasites and the induced hyperplasia remain restricted to the tips, leaving the remaining filament functional. Mortality never occurred in fish longer than 32–35 mm, which survived heavy infections as high as 300 parasites per fish (Paperna, 1963b).
Acolpenteron ureteroecetes infecting the ureter of Micropterus salmoides causes inflammatory changes. Acute conditions were accompanied by dropsy and chronic infection of the ureter leads to blockage swelling and deposition of a crystalline precipitate. Degenerative and necrotic changes also extend to the posterior end of the kidney (Du Plessis, 1948).
There are no records of ill effects due to dactylogyrid infections in cichlids in Africa or Israel, even when infections are high. However, of the five monogeneans introduced with Oreochromis spp. to Southeast Asia, one of these, Cichlidogyrus sclerosus, has been reported to harm cultured fish (Kabata, 1985).
Some of the species of Quadriacanthus infecting clariid catfish are apparently also potentially pathogenic and morbid infections with unidentified species were reported from farmed catfish (Clarias batranchus) in Southeast Asia (Kabata, 1985).
In eels (Anguilla spp.), reared in warm water farming systems and infected with Pseudodactylogyrus anguillae and P. bini, the mouth and branchial zone, as well as the gills become hyperemic, there is increased mucus secretion, and erosion of the lamellar texture or, in other cases, extensive hyperplasia of the gill epithelium (Chan & Wu, 1984; Buchmann et al., 1987).
Fish heavily infected with Gyrodactylus appear pale, due to excessive mucus secretion and epithelial proliferation. In the more heavily infected skin zones, there is skin erosion; desquamation of the skin epithelium, focal haemorrhagic lesions and loss of scales (Tripathi, 1957; Gopalakrishnan, 1963; Kabata, 1985). Obiekezie & Taege (1991) reported severe mortalities (up to 90%) of Clarias gariepinus fry (two weeks old) in a hatchery in Nigeria, due to a severe infestation by Gyrodactylus groschafti. Khalil (1964) reported fatal hyperinfections (690–7340 worms per fish) by Macrogyrodactylus polypteri of aquarium held Polypterus senegalus. Species of Macrogyrodactylus occur in fish with potential for aquaculture in Africa, Clarias spp., Lates niloticus and Anabantidae (Paperna, 1979).
Spontaneous decline of infection has been reported in both dactylogyrid and gyrodactylid infections. Surviving Carp fingerlings (31–61 mm long) spontaneously recovering from D. vastator infection in ponds, resisted reinfection for about 40 days after its onset. Fish, reared free of infection to the size of 65–80 mm became readily infected when exposed, but infection in such fish never lasted more than 12 days (Paperna, 1964c).
Spontaneous recovery of P. senegalus from Macrogyrodactylus polypteri infection occurred after two weeks (Khalil, 1964).
Injections of hydrocortisone caused elevation of infection levels in Oreochromis spp. with both Cichlidogyrus sclerosus and Gyrodactylus sp. (Shaharon-Harrison, 1987).
Monogeneans, Dactylogyridae in particular, are highly host specific, and seem to have co-evolved with their hosts. The same parasite species, however, often infects several fish species of the same genus or species group, and parasites occurring on the host of the same fish family are taxonomically related, usually at the generic level (example: Cichlidogyrus and Cichlidae). Such co-evolutionary relationships are less evident in Gyrodactylidae in which species of the same genera (e.g. Gyrodactylus, Macro-gyrodactylus) occur in representatives of diverse fish families, although individual species, if correctly determined, seem to be narrowly host specific (Malmberg, 1970); this also applies to species infecting African fish (Paperna, 1979). Among species of Polypterus, only P. senegalus succumbed to massive infestation of Macrogyrodactylus polypteri; all others exposed under similar conditions became only lightly infected (Khalil, 1964).
In most fish species associated with monogeneans, incidence is high (approaching 100%) and intensities of 20–100 or more worms per fish are common (Paperna, 1964a, 1979; Batra, 1984). Crowding fish into culture systems or aquaria often promotes infestation. Introduction of Polypterus senegalus into aquaria caused an exponential increase in infestations with Macrogyrodactylus polypteri, resulting in a worm burden of 690–7340 per fish within 20–25 days. Natural infections of the same fish species and parasites in the Nile did not exceed 6 worms per single fish (Khalil, 1964). In small habitats and culture systems, the predicted increase in infestation is, however, not always fulfilled, due to the inhibitive quality of physical (depth, currents, temperatures) and chemical (oxygen, salinities) factors of the environment. In such habitats, decline has also been observed in the diversity of the monogenean species, for example, cichlids usually infected with a variety of species, becoming infected by a single species only (C. arthracanthus in T. zillii and either C. tilapiae or C. sclerosus in Oreochromis spp.) (Paperna, 1963d, 1979).
Species of dactylogyrids as well as gyrodactylids demonstrate different tolerances to water salinity. Particularly tolerant to euryhaline waters are D. extensus (infecting carp) (Paperna, 1964a) and G. cichlidarum (infecting cichlids) which are tolerant to water of 1 ppt salinity.
Heavy infections of Diplectanus lacustris occur in introduced Nile perch in Lake Kyoga and the Victoria Nile, while being low in Nile perch in their native Lake Albert.
Massive mortalities due to heavy urethral infection by Acolpenteron ureteroecetes in hatchery reared, introduced Micropterus salmoides were reported in South Africa (Du Plessis, 1948).
Species of Dactylogyrus are often introduced with carp. European populations of D. anchoratus, D. minutus and D. vastator infecting carp are thermophilic, with optimal reproduction at ambient water temperatures of 28–29°C, while the high oxygen demand of the developing eggs of D. extensus causes a decline in hatching rate at elevated ambient temperatures (from 75% at 14°C to 9% at 20°C) and results in an optimal rate of reproduction at 17°C ambient water temperature (Izumova, 1958; Bauer, 1959). D. extensus, as well as all other introduced Dactylogyrus spp., however, become well adapted and thrive in the eutrophic warm water conditions of Israeli fish ponds (28–30°C, and dissolved oxygen at times declining to 0.4 mg/l) (Paperna, 1964a).
Heavy infestations by D. vastator caused mass mortality of carp fry (<35 mm in length) during the spawning season (spring to early summer) in breeding and nursery ponds in Israel. Epizootiological investigation of the circumstances under which these mortalities occurred revealed the following (Paperna, 1963a):
Mortalities only occurred in ponds which were used every year to rear fry, and most often in ponds where mortalities had been recorded in preceding years.
The fish population density of affected ponds was always above 5 million fry per hectare (about 0.25 kg biomass per 1m3). Daily growth increments of fry in such ponds were less than 1 mm (sometimes only 0.5 mm), compared with a daily growth increment of 1.3–1.6 mm in low density (<500,000 fry/hectare) ponds.
Parasites appeared simultaneously by mid-April in fry-stocked ponds of different regions and farms. Mortalities usually occurred 25–35 days after spawning, in 18–26 mm fish. Survivors of the mortalities in the ponds gradually lose the infection. Mortalities never occurred, irrespective of stocking density, in ponds where infection had not been established soon after spawning. Delay in establishment of infection (10–44 days post-spawn) occurred in ponds spawned prior to April (where a warm [20–24°C] ground water supply is available) or in ponds not used for fry production in previous years.
Circumstantial evidence suggests that infection originated annually from “resting” eggs remaining in the ponds from the previous year's growing season. Parasites were never found on fish other than fry and fingerlings or outside the breeding season (August–April) (Paperna, 1963a,b).
Growth conditions in the ponds - water quality and stocking densities are the predisposing factors to infections and losses of carp due to D. extensus (Bauer, 1959; Sarig, 1971), grass carp due to D. lamellatus and bighead carp (Aristichthys nobilis due to D. nobilis (Molnar, 1971; Bauer et al., 1969; Shaharom-Harrison, 1986). The same applies to infections by Pseudodactylogyrus spp. of eels farmed in warm water systems (Chan & Woo, 1984; Buchmann et al., 1987).
Epizootic gill infections by D. baueri and D. formosus and skin and gill infections with Gyrodactylus medius occur in commercially reared goldfish during overcrowding in tanks before marketing. In Israel, heavy infections of hatchery hybrid ‘tilapia’ fry by Cichlidogyrus spp. combined with epizootic infestations of trichodines and Tripartiella cichlidarum were suggested to be pathogenic (Landsberg, 1989). Overwintering tilapia in ponds are concurrently infected by Gyrodactylus cichlidarum and Chilodonella spp. In carp, heavy gyrodactylosis was seen in fish with skin papiloma. Clinical Gyrodactylus infections have been reported also to trouble intensively farmed ‘tilapia’ in Kenya. Mortalities associated with epizooties were reported to occur two weeks after handling and transfers (Roberts & Sommerville, 1982).
Infections of Dactylogyrus spp. in carp fry and fingerlings in earth ponds are controlled through application of 0.12 ppm (A.I.) Bromex (Dibrom, Naled). Repetition of treatment within a week is recommended. The safety index for carp fry is 32 (Sarig, 1971). Elsewhere another organophosphate -- Masoten (Dipterex, Neguvon, Dylox) is used at a dose of 0.25–0.50 ppm (A.I.). The safety index for carp fry is 12 (Sarig et al., 1965; Schmahl, 1991). Quick treatment with a mixture of 2 ppm of 50% DDVP (DP, dichlorovos, Vapona), 0.2 ppm Bromex and 25 ppm Formalin (36% Formaldehyde) for 4–6 hours has been recommended to clear ‘tilapia’ fry in hatchery tanks infested with both Cichlidogyrus and trichodines (Landsberg, 1989). The same treatment has been applied to Gyrodactylus infections. Some populations of Gyrodactylus elegans in goldfish, however, demonstrated an apparent resistance to a dosage as high as 12.5 ppm and in some instances also 25 ppm (Goven et al., 1980). A resistance to bromex seems to be also developing among Gyrodactylus medius infecting commercially farmed goldfish in Israel.
Recently the use of Praziquantel has been advocated (a 3 hour bath in 10 mg/l solution at 22°C - Schmahl & Mehlhorn, 1985) and data were provided on the efficacy of other anthelminthic drugs such as Levamisol (2h bath in 50 ml/l), Niclosamide (2 h bath in 0.075–0.1 ml) and Mebendazole (24h bath of 1 mg/l) (Schmahl, 1991). Praziquantel is at present too expensive for commercial use, the other drugs need more extensive testing before being considered for routine use.
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Plate 20. Dactylogyrid Monogenea: a. Dactylogyrus vastator carp fry from a pond, Israel (0.9 mm long). b. Diplectanum lacustris ‘gravid’ form (1.5 mm long) on gill filament tip of Lates niloticus, northern L. Victoria. c. Enterogyrus cichlidarum from stomach of Tilapia zillii, Israel (280 mm long); A. Anchors, B. Bars, C. Copulatory organ. E. Eyes, O. Opisthaptor, P. Prohaptor. d. Pre-mature (transparent, J) and mature (filled with granular vitellaria) D. vastator inducing epithelial proliferation (Hp) in gills of carp fry. e. Dactylogyrus anchoratus infesting gills of young carp. f. Anchors (A), Bars (B) and hooklets (H) in the opisthaptor of Quadriacanthus clariadis, from Clarias gariepinus, L. Victoria.
Plate 21. Gyrodactylid Monogenea: a. G. mugili from Mugil saliens skin from an Israeli Mediterranean estuarine habitat, life (arrow intrauterine offspring). b. Scanning electron micrographs (SEM) of G. cf. medius from farmed goldfish, Israel. c. Details of opisthaptor attachment of b. d. SEM of G. cichlidarum from skin of Israeli farmed tilapia hybrids. e. Opisthaptor of G. cichlidarum from Oreochromis sp. from Uganda, life. f. SEM details of opisthaptor of d. SEM details of opisthaptor of G. cichlidarum from O. leucostictus, Lake Naivasha, Kenya.
Fig. 3a. Monogenea: A. General view of Cichlidogyrus arthracanthus (400 μm long) from Tilapia zillii. B–W. Ophisthaptoral armature of species representing major genera of African Dactylogyroidea: B. Cichlidogyrus halli, hosts: Oreochromis and Sarotherodon spp. C. Onchobdella voltensis, hosts: Hemichromis spp. D. Diplectanum lacustris, hosts: Lates spp. E. Dogielus dublicornis, host: Labeo cylindricus. F. Dactylogyrus afrofluviatilis, hosts: Barbus spp. G. Acolpenteron pavlovskii, host: Cyprinus carpio. H. Heterotesia voltae, Host: Heterotis niloticus. I. Jainus (=Characidotrema) longipenis, host: Alestes leuciscus. J. Ancyrocephalus s.l. synodontis, hosts: Synodontis spp. K. Quadriacanthus clariadis, hosts: Clarias, Heterobranchus and Bagrus spp. L. Bagrobdella auchenoglanii, host: Auchenoglanis occidentalis. M. Protoancylodiscoides chrysichthes, host: Chrysichthys nigrodigitatus. N. Schilbetrema acornis, host: Schilbe mystus. O. Schilbetrema bicornis, host: Physalia pellucida. P. Eutrianchoratus magnum, host: Ophiocephalus obscurus.
Fig. 3b. Monogenea continued: Q. Ancyrocephalus s.l. barilii, hosts: Barilius spp. R. Afrocleidodiscus paracleidodiscus, host: Distichodus niloticus (another species on Hydrocynus spp.). T. Annulotrema gravis, hosts: Alestes spp. U. Nanotrema citharini, host: Citharinus citharus. V. Ancyrocephalus s.l. pellonulae, host: Pellonula afzeliusi. W. Macrogyrodactylus ctenopomae, host: Ctenopoma muriei. X. Diplozoon aegyptiensis general view (× 20). Y. Neodiplozoon polycotyleus, general view (× 60).
Plate 20. Dactylogyrid Monogenea (legend p. 116).
Plate 21. Gyrodactylid Monogenea (legend p. 116).
Fig. 3a. Monogenea (legend p. 117).
Fig. 3b. Monogenea continued (legend p. 117).