New findings of trematodes of the superfamily Echinostomatoidea Looss, 1899 in birds from the Czech Republic

Adult echinostomatoids fl ukes occur in different groups of vertebrates, the cercariae in snails and metacercariae in molluscs (Gastropoda, Bivalvia), planarians, fi shs and tadpoles. Therefore, in Europe echinostomatoids are most frequent in water birds but rare in birds of prey and owls. Sometimes, they can be found also in songbirds of the families Corvidae and Turdidae, as some crows and thrushes occasionally feed on aquatic mollusks, fish and amphibians.

The systematics of the superfamily Echinostomatoidea was detailed in the work of Kostadinova (2005). The fauna of bird echinostomatoids is relatively well known in the Central Europe; Sitko et al. (2006) published the survey of the bird trematodes in the Czech Republic and Slovakia, Iskova (1985) summarized echinostomatoids trematodes in Ukraine, and Sonin (1985) studied this fl uke group in fi sh-eating birds of the Palearctic region. However, updating these data is diffi cult because the diversity and abundance of birds have a long downward trend (Rosenberg et al., 2019).

During the years 2015 – 2019, 12 birds of four species were examined. They were six Caspian gulls Larus cachinnans (Lariformes), three goosanders Mergus merganser (Anseriformes), two common snipes Gallinago gallinago, and one common curlew Numenius arquata (Charadriiformes). The birds were provided from the Wild Animal Rescue Stations in Bartošovice na Moravě and Přerov, Czech Republic (Stýblo & Orel, 2013). All the birds were found dead or died of injury; several water birds died caused by botulism on the ponds. Trematodes were fixed in 70 % ethanol, stained by Borax-carmine, transferred through ethanol series to xylene and mounted in Canada balsam. All measurements are in micrometres. Documentary material is deposited in the helminth collection of the Comenius Museum at Přerov, Czech Republic.

The research related to animals complied with all the relevant national regulations and institutional policies for the care and use of animals.

Aporchis massiliensis Timon-David, 1955 Fig. 1a, b

Fig.1a

Host: Larus cachinnans Pallas (Lariformes).

Prevalence: one positive out of six host birds.

Site: intestine.

Locality: Sedlec u Mikulova (48.86ºN, 19.16ºE; 7266).

Specimens deposited: P–P–1858/53.

Remarks: previously found in France (Timon-David, 1955), UK (Pemberton, 1963), Spain (Bosch et al., 2000), Italy (Lafuente et al., 1998), Egypt (Radwan et al., 2013), Russia (Kirilov & Kirilova, 2013). Hosts: Larus argentatus, L. cachinnans, L. fuscus, Ichthyaetus audouinii, I. leucophthalmus, I. melanocephalus, Chroicocephalus ridibundus, Chlidonias leucoptera and Sterna hirundo. The species is characterized by a head disc measuring about 300, vitelline field ending at the rear edge of the ovary and egg filaments about 500 long. The number of spines could be accurately determined. Only clearly visible spines are shown. The bird was frozen before the autopsy. Present record represents the first finding in Central Europe.

Description (one specimen): Body 20,000 long, greatest width in region of ovary 714 (BW=6 %). Forebody notably short, 238 long, hindebody 19,443 (FO=2 %). Anterior part of body up to level of beginning vitelline field strewn with minute spines. Kidney shaped disc 255 × 313. Angle spines 32 × 12, dorsal lateral spines 15 × 6, dorsal oral spines 2 × 2. Oral sucker terminal 110 × 93. Prepharynx 17, pharynx long oval close behind oral sucker 110 × 81, oesophagus 203. Ventral sucker well developed 319 × 290. Cirrus pouch 1267 × 75. Intestine well developed, its bifurcation close to ventral sucker. Individual branches end at level of end of body, far behind ends of vitelline field feebly developed, contrary to remaining species of this family. They begin in posterior third of body and end before reproductive organs. As a rule, one of their branches begins considerably lower than other branch. Outlets of vitelline field and vitelline follicle, as long as developed, in region of ovary. Testes well developed, long oval, medially in tandem, anterior testis 534 × 368, posterior one 644×368 (T=6 %). Ovary spherical or ovoid, laterally at end of vitelline field, partly overlaid by loops of uterus, 344 × 232. Mehlis’ gland well developed, 232 × 203. Uterus well developed (U=33 %), occupy whole space between ovary and margins of vitelline field, in anterior part of body reaching in front of vitelline field. Eggs 99 × 35, provided with long filament 500 – 510 (500).

Echinoparyphium macrovitellatum Oschmarin, 1947 Fig. 2a, b

Fig. 2a

Host: Larus cachinnans Pallas (Lariformes).

Prevalence: one positive out of six host birds.

Site: intestine.

Locality: Záhlinice (49.29ºN, 17.48ºE; 6770).

Remarks: described from Phalacrocorax carbo in Eastern Siberia (Sonin, 1985), Microcarbo pygmaeus and Pelecanus onocrotalus in Azerbaijan (Vaidova, 1978). The species is characterized by small size, a head disc with 29 spines and vitelline field composed of large follicles. In Europe described for the first time.

Description (5 specimens): Body fusiform 1,086 – 1,386 (1225) long, maximum width 224 – 268 (239) occurring at testes, (BW=17–20 %). Forebody 368 – 522 (429), hindbody 596 – 894 (706), (FO=33–38 %). Anterior body surface covered with spines 10 – 14 (12) × 1 – 3 (2) which become rare and disappear behind ventral sucker. Head collar 116 – 122 (118) × 145 – 174 (157) bears 29 spines in two row. Angle spines 53 – 58 (55) × 12 – 14 (13). Dorsal lateral spines 34 – 36 (35) × 10 – 12 (11), dorsal oral spines 34 – 36 (34) × 10 – 12 (11). Oral sucker slightly protruding 62 – 70 (67) × 62 – 74 (69). Prepharynx absent, or 12 – 19 (13), elongated oval pharynx 62 – 75 (68) × 46 – 58 (51) continues into oesophagus 174 – 180 (177). Ventral sucker round or widely oval 139 – 154 (150) × 139 – 154 (152) at posterior half of body. Ratio of sucker length 1: 1.99 – 2.22 (2.12), width 1: 1.99 – 2.34 (2,2). Testes smooth, elongated transversely, compact, in tandem at posterior body half, anterior testis 116 – 157 (141) × 145 – 174 (152), posterior testis 145 – 203 (170) × 145 – 186 (160) (T=23– 27 %). Cirrus pouch oval 197 – 209 (203) × 116 – 122 (120), dorsally between bifurcation of intestine and centre of ventral sucker, cirrus 116 – 177 (154±6) × 35 – 61 (47). Ovary oval or circular 70 – 87 (76) × 70 – 87 (76) in right part of body between ventral sucker and anterior testes. Mehlis´ gland diffuse 58 – 70 (67) × 64 – 70 (67). Vitelline field composed of large follicles at posterior end of anterior testes and reaching posterior end of body, behind testes fill up whole body space with exception of narrow strip in middle, left branch 662 – 894 (724), right branch 662 – 854 (712). Uterus short (U=6–13), with few 3 – 6 (4±2) oval eggs 81 – 87 (83) × 58 – 60 (59).

Echinostoma academica Skrjabin, 1915 Fig.3a, b

Fig.3a

Host: Numenius arquata (L.) (Charadriiformes).

Prevalence: one positive out of one host bird.

Site: intestine.

Locality: Přerov (49.45ºN, 17.46ºE, 6570).

Specimens deposited: P–P–1858/42.

Remarks: found in Russia from Charadiiformes – Limosa limosa, Gallinago media (Bykhovskaya-Pavlovskaya, 1962), Crocethia alba (Ivanov et al., 2013), Poland from

Numenius arquata (Okulewicz et al., 2010), Ukraine from Ralliformes – Rallus aquaticus (Iskova, 1985). The species is characterized by a head disc with 43 spines and tegumental spines extending to the ovary area. The present record represents the first finding in Czech Republic.

Description (10 specimens): Body 7,436 – 10,860 (8,530) × 800 – 1,143 (1,003) width occurring at testes (BW=9–14 %).Forebody 1114 – 1629 (1362), hindebody 5710 – 8530 (6723) (FO=13– 19 %). Anterior body surface covered with spines 7 – 12 (9) × 2 – 5 (4), which become rare and disappear behind ventral sucker. Head collar reniform 368 – 744 (508) × 492 – 782 (654) bears 43 spines. Angle spines 122 – 145 (134) × 29 – 35 (33). Dorsal lateral spines in double row 81 – 110 (100) × 23 – 29 (27), dorsal oral spines 79 – 89 (86) × 21 – 24 (22). Oral sucker subterminal, small 191 – 290 (243) × 203 – 278 (240). Prepharynx short 58 – 138 (81), pharynx well developed 162 – 203 (186) × 133 – 162 (147), oesophagus short, 406 – 690 (603). Ventral sucker large with deep cavity 506 – 708 (614) × 534 – 820 (698). Ratio of sucker length 1: 2.07 – 3.12 (2.60), width 1: 2.32 – 3.53 (2.92). Testes in tandem, elongate oval, anterior testis 368 – 515 (430) × 184 – 276 (225), posterior testis 442 – 653 (530) × 202 – 322 (257) (T=11–13 %). Cirrus pouch oval to elongate oval, muscular between intestine bifurcation and posterior margin of ventral sucker, dorsally 232 – 644 (484) × 230 – 322 (257). Internal seminal vesicle large, with saccular posterior part and coiled tubular anterior part. Pars prostatica well developed. Ejaculatory duct long. Cirrus tubular, unspined. Ovary small, spherical, median 230 – 276 (256) × 184 – 276 (236). Mehlis´ gland muscular, 147 – 368 (286) × 147 – 276 (213). Vitelline field with small follicles, left 5,146 – 8,299 (6,012), right 4,290 – 8,170 (5,866). Uterus long with numerous loops (U=21– 36 %). Eggs 104 – 116 (111) × 58 – 70 (66).

Echinostoma stantschinskii Semenov, 1927 Fig. 4a,b

Fig.4a

Host: Gallinago gallinago (L.) (Charadriiformes).

Prevalence: one positive out of two host birds.

Site: intestine.

Locality: Tovačov (49.42ºN, 17.25ºE; 6569).

Specimens deposited: P–P–1858/44.

Remarks: Characteristic parasite from Gallinago gallinago, found in Russia (Sonin, 1985), Azerbaijan (Vaidova, 1978), Kyrgyzstan (Tokobaev & Chibichenko, 1978), Ukraine (Iskova 1985), Poland (Pojmanska et al., 2007). The species is characterized by a head disc with 32 – 33 spines, 5 angle spines and small eggs around 80 × 45. The present record represents the first finding in Czech Republic.

Description (5 specimens): Body 7,430 – 8,000 (7,712) × 914 – 1,000 (964) width occurring at testes (BW=12–13 %). Forebody 1,000 – 1,200 (1,082), hindbody 5,430 – 5,910 (5,713) (FO=12–15 %). Anterior body surface covered with spines 12 – 17 (14) × 2 – 3 (2), which become rare and disappear behind ventral sucker. Head collar renal 460 – 506 (478) × 644 – 828 (598) bears 32 – 33 spines. Angle spines 96 – 100 (98) × 23 – 29 (26). Dorsal lateral spines in double row 87 – 96 (92) × 26 – 29 (28). Dorsal oral spines 84 – 87 (86) × 22 – 26 (24). Oral sucker subterminal, small 203 – 261 (234) × 261 – 278 (264). Prepharynx short 29 – 58 (43), pharynx well developed 203 – 232 (216) × 157 – 197 (174), oesophagus short, 460 – 644 (542). Ventral sucker large with deep cavity 736 – 894 (830) × 736 – 894 (836). Ratio of sucker length 1: 3.35 – 3.85 (3.55), width 1: 2.82 – 3.43 (3.17). Testes tandem, elongate oval, anterior testis 644 – 874 (750) × 322 – 386 (340), posterior testis 690 – 1,013 (845) × 286 – 414 (332) (T=18–21 %). Cirrus pouch oval to elongate oval, muscular between intestine bifurcation and posterior margin of ventral sucker, dorsally 368 – 894 (599±137) × 276 – 460 (362±67). Internal seminal vesicle large, with saccular posterior part and coiled tubular anterior part. Pars prostatica well developed. Ejaculatory duct long. Cirrus tubular, without spine. Ovary small, spherical, median 368 – 460 (418) × 322 – 377 (357). Mehlis´ gland muscular, 230 – 368 (304) × 368 – 414 (383). Vitelline field with small follicles, left 2,860 – 5,140 (3,602), right 2,860 – 4,860 (3,474). Uterus long with numerous loops (U=16–24 %). Eggs 80 – 85 (83) × 40 – 45 (43).

Echinochasmus mergi (Cannon, 1938) Fig. 5a, b

Fig.5a

Host: Mergus merganser L. (Anseriformes).

Prevalence: one positive out of three host birds.

Site: intestine.

Locality: Záhlinice (49.29ºN, 17.48ºE; 6770).

Specimens deposited: P–P–1858/48.

Remarks: Found in Canada (Yamaguti, 1971) and Germany from Mergus merganser (Odening, 1963). The species has a head disk with 22 spines, prepharynx is longer than the oral sucker, vitelline field of large follicles connect behind the testes. The present record represents the first finding in Czech Republic.

Description (6 specimens): Body 1,386 – 1,490 (1,453) × 238 – 286 (267) width occurring at testes (BW=16–20 %). Forebody 644 – 715 (681), hindbody 581 – 700 (634), (FO=44–50 %). Anterior body surface covered with spines 12 – 17 (14±2) × 2 – 5 (2±1), which become rare and disappear behind ventral sucker. Head collar renal 209 – 249 (227) × 215 – 232 (232) bears 22 spines in one row. Angle spines 38 – 50 (48) × 12 – 14 (13), dorsal lateral spines 60 – 65 (62) × 14 – 17 (16), dorsal oral spines 55 – 60 (58) × 15 – 17 (16). Oral sucker subterminal, small 64 – 75 (69) × 58 – 75 (66). Prepharynx 75 – 87 (78), pharynx well developed 87 – 110 (99) × 52 – 60 (57), oesophagus 348 – 452 (402). Ventral sucker large with deep cavity 116 – 174 (142) × 128 – 157 (144). Ratio of sucker length 1: 1.73 – 2.49 (2.05), width 1: 1.83 – 2.50 (2.20). Testes tandem, elongate oval, anterior testis 70 – 174 (108) × 116 – 203 (152), posterior testis 104 – 174 (133) × 116 – 203 (152) (T=13–24 %). Cirrus pouch oval to elongate oval, between intestine bifurcation and posterior margin of ventral sucker, dorsally 87 – 128 (108) × 64 – 93 (78). Internal seminal vesicle large, with saccular posterior part and coiled tubular anterior part. Pars prostatica well developed. Ejaculatory duct long. Ovary small, spherical, median 58 – 70 (68) × 58 – 70 (60). Mehlis´ gland 58 – 70 (64) × 58 – 70 (65). Vitelline field with small follicles, left 477 – 598 (559), right 536 – 598 (572). Uterus short with a small number of eggs (U=8–13 %). Eggs 75 – 93 (82) × 50 – 58 (56).