I. Acanthocephalus Anguillae (Palaeacanthocephala) in Naturally Infected Fishes: LM and TEM Investigations
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DISEASES OF AQUATIC ORGANISMS Vol. 4: 109-1 19, 1988 Published May 31 Dis. aquat. Org. Host-parasite interface of fish acanthocephalans. I. Acanthocephalus anguillae (Palaeacanthocephala) in naturally infected fishes: LM and TEM investigations Horst Taraschewski Institut fiir Spezielle Zoologie und Parasitologie, Ruhr-Universitlt-Bochum, D-4630 Bochum, Federal Republic of Germany ABSTRACT: Nine species of freshwater fish from Ruhrlake (FRG) were investigated for infection with Acanthocephalus angdlae over 2 yr Prevalence rates of infected fish did not depend on season and were as follows: Leuascus cephalus (chub) 84 7'0, Tinca tinca (tench) 44 %, Abramis brama (bream) 34 %, Angullla anguilla (eel)30 %, Rutrlus rutilus (roach) 16 '10,Alburnus alburnus (bleak) 15 %. Mean intensities ranged from 1 to 7 worms per fish. Chub was the major host in terms of both prevalence and intensity of infection. For investigations on the host-parasite interface Salmo trutta (brown trout), S. gairdneri (rainbow trout) and Leuciscus leuciscus [dace) from other biotopes were also included. In chub, tench, eel, dace and bleak the worms penetrated the intestinal wall by their presoma up to the muscularis or even perforated it completely. In these hosts, living or dead worms were also found within the peritonea1 cavlty and/or viscera. In roach and bream the worms did not penetrate the muscularis, whereas in brown and rainbow trout they never penetrated the stratum compactum. The hosts' inflammatory tissue consisted of 3 zones. The first layer, of necrotic cells and degranulated granulo- cytes, was found adjacent to the surface of the parasite. Thls necrotic zone gradually passed over to a second layer of mostly intact eosinophdic and heterophlic granulocytes and fibroblasts. The third and outermost layer consisted of collagenous fibers and a few fibroblasts and granulocytes. The fibrous outer layer was only found in those hosts where the worms penetrated the muscularis. A semiliquid, osmiophilic layer between worm-presoma and host tissue was conspicuous in all fish species. INTRODUCTION mainly confined to light microscopical studies except for a scanning electron microscopical examination of During the last 50 yr numerous papers have dealt the rat intestine experimentally infected with with the histopathology of acanthocephalans in fish, Moniliforrnis rnoniliformis (Martin et al. 1983). most based on paraffin sections of species from natur- httle information on the fine structure of acan- ally infected hosts (Steinstrasser 1936, Wurmbach thocephalan probosces and presomas is available, 1937, Prakash & Adams 1960, Bullock 1963, Chaicharn although the proboscis with its hooks is in most inti- & Bullock 1967, Esch & Huffines 1973, Schmidt et al. mate contact with the host's tissue and defense cells. 1974, George & Nakadal 1981, 1982, McDonough & Hammond (1967) described the proboscis tegument of Gleason 1981).Recently Wanstall et al. (1986) reported Acanthocephalus ranae and Hutton & Oetinger (1980) electron microscopical results on Pomphorhynchus the proboscis hooks of larval MoniLiforrnis rnoniliformis. laevisin experimentally infected rainbow trout. Investi- The present article is the first of a series of compara- gations on acanthocephalan histopathology in birds tive Light microscope (LM), scanning electron micro- (Pflugfelder 1956, Moore & Bell 1983) and mammals scope (SEM) and transmission electron microscope (Chandler 1953, Takos & Thomas 1958, Richart & (TEM) investigations on the host-parasite interface of Benirschke 1963, Moore 1979, Tesana et al. 1982, Leng fish acanthocephalans in naturally and experimentally et al. 1983, Nelson & Nick01 1986) have also been infected final hosts, and of descriptions of the proboscis O Inter-Research/Printed in F. R. Germany Table 1 Acanthocephalus anguillae. Prevalence and intensity of infection in 9 fish species from Ruhrlake from 26 Nov 1984 to 15 Dec 1986 (disintegrating extraintestinal worms not counted) Host species n Sampling Mean Mean Mean Infection Mean no. Approximate No. of fish double-infected season length length of length of rate worms per max, length by other acanthocephalans [cm1 uninfected infected i0/o I inf. fish of worms (intensity: range) (range) fish fish (range) [cm] Chub Leuciscus cephalus 101 All seasons 29.0 27.7 29.3 84.2 6.6 4 4 Pornphorhynchus laevis (13.7-41.0) (1-35) (1-2) Tench Tinca tinca 11 All seasons 33.6 35.3 32.6 45.5 2.1 2 2 P. laevis (1-2) (15.2-41.0) (1-3) 1 Acanlhocephalus lucii (1) Bream Abraniis brarna 190 All seasons 23.2 23.5 34.2 2.6 1 Echinorhynchus truttae (15.0-50.5) (1-12) (1) Eel Anguilla anguilla 57 Jun-Jul 40.4 40.7 29.9 5.9 9 A. lucii (14) 85 & 86 (25.2-56.0) (1-29) Roach RLILJILISrulilus 83 1 Oct-31 Mar 21.3 21.2 13.7 5.6 - (1-30) Roach 188 1 Apr-30 Sep 19.4 19.5 17.0 2.3 (1-9) Roach 271 AU seasons 19.9 20.0 15.5 3.1 (10.5-30.0) (1-30) Bleak Albrlrnus alburnus 55 All seasons 12.9 12.7 14.5 1 (10.5-18.0) (1) Stone perch Acerina cernua 7 All seasons 14.1 14.1 14.3 6 5 A. lucii (1-8) (12.5-17.0) (6) Perch Perca fluviatilis 43 All seasons 22.0 22.0 0 - 31 A. lucii (140) (11.2-26.5) Pike Esox lucius 2 All seasons 75.5 75.5 - 0 1 A. lucii (16) (61.0-90.0) Taraschewski: Acanthocephalan naturally infecting fishes ultrastructure. Acanthocephalus anguillae is the most RESULTS widespread fish acanthocephalan in Germany (Tara- schewski 1985) and is thus considered first. Field data Field studies on A. anyuillae in naturally lnfected chub are treated here, but detailed results on the host-parasite interface Prevalences and intensities of infection with Acan- for this species will be published elsewhere (Tara- thocephalus anguillae in 9 host species from Ruhrlake schewski unpubl.). are given in Table 1. There was neither a seasonal variation m infection (shown only for roach in the table) nor a relation between fish length and infection rate. MATERIALS AND METHODS Among the 9 species of fish only perch and pike were never infected with A, anguillae (dace, brown and Hosts and parasites. Fish naturally infected with rainbow trout did not occur in the Ruhrlake). All the Acanthocephalus anguillae were used exclusively in other species were infected. Chub was most frequently this study. Nine species of fish (Table 1) were collected infected and harboured the highest numbers of worms. in the Federal Republic of Germany from the artificial In addition, female worms from chub measured up to Ruhrlake (Kemnader See) near Bochum, while from the 4 cm in length while worms from other hosts were river Lippe near Hamm, only dace Leuciscus leuciscus smaller. Perch, stone perch and pike were more fre- were collected; brown trout Salmo trutta and rainbow quently infected with Acanthocephalus lucii than with trout S. gairdneri were obtained from the river Lein- A. anguillae (Table 1). bach near Heilbronn. Dace and the 2 species of trout did not occur in the Ruhrlake. All fish were transported alive to the laboratory in Bochum, where they were Host-parasite interface kept for up to 2 d. After killing, the fish were opened immediately. The size of A. anguillae individuals con- In general female worms provoked a more pro- tained within the intestine or viscera was estimated by nounced host reaction than males (Fig. 1). The hosts naked eye. For quantitative evaluation of infections, could be divided into 3 groups based on the depth of only fishes from the Ruhrlake were used. It was estab- the worms' penetration into the intestinal wall. lished that A. anguillae was the main acanthocephalan species during all seasons and in all 3 biotopes. Intesti- nal samples with attached worms were taken from the Group 1 hosts immediately after their death and treated as described below. In eel (Figs. 5 and 6) and in the 3 cyprinids - tench Light microscopy. Squash preparations of intestinal (Figs. 2, 7 and 8),dace (Fig. 11) and bleak - the worms samples (of about 3 cm in length) were photographed had deeply penetrated the hosts' intestinal wall, either between 2 glass plates. Pieces of up to 1 cm in diameter with the presoma alone or together with the anterior containing a presoma of Acanthocephalus anguillae metasoma. Worms from these 4 hosts usually broke off were fixed in Bouin's solution, embedded in paraffin, at the neck when pulling them out of the intestinal sectioned at 5 to 7 pm and stained with Azan-stain or wall. In these hosts whole worms were also found aldehyde-fuchsin stain after Goldner (Burck 1982).The inside the peritonea1 cavity (Fig. 2) or inside the vis- descriptions are based on 5 worms from each host cera. Such extraintestinal worms were either enclosed species. by a precipitin-like coat (Fig. 2) or by proliferate host Electron microscopy. The worm's trunk was cut off tissue. The same applied to chub, but these results will behind the neck region, and portions of the fish's gut of be published elsewhere (Taraschewski unpubl.). All up to 3 mm around the worm's point of attachment investigated specimens of tench harboured several, were fixed in 5 O/O glutaraldehyde buffered with 0.1 M mostly dead, worms in extraintestinal locations which, sodium cacodylate, pH 7.4 at 4 'C for 24 h. Postfixation however, were difficult to count, since most of them was done in 2 % OsOl in the same buffer. Samples were already highly disintegrated. were dehydrated in a graded ethanol series, trans- Eel. Most female worms had destroyed the mucosal ferred to propylene oxide and embedded in Araldite. epithelium, the circular musculature, the overlying lon- Semithin sections were stained with methylene blue gitudinal musculature and the serosa.