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Morphological polymorphism in tapeworms: redescription of Caryophyllaeus laticeps (Pallas, 1781)(Cestoda: Caryophyllidea) and characterisation of its morphotypes from different fish hosts

Vladimíra Hanzelová • Mikuláš Oros • Daniel Barčák • Dana Miklisová • Diana Kirin • Tomáš Scholz

V. Hanzelová • M.Oros • D. Barčák • D. Miklisová

Institute of Parasitology, Slovak Academy of Sciences, Hlinkova 3, 04001 Košice, Slovakia

D. Kirin

Agricultural University of Plovdiv, 12 Mendeleev Street, 4000 Plovdiv, Bulgaria

Tomáš Scholz ()

Institute of Parasitology, Biology Centre of the Academy of Sciences of the Czech Republic, Branišovská 31, 370 05 České Budějovice, Czech Republic

e-mail:

List of the specimens of Caryophyllaeus laticeps (Pallas, 1781) studied

Morphotype 1

(i) Specimens from museum collections: 16 specimens from Abramis brama, Rivers Danube, Hron, Latorica and Tisa, Slovakia, 1958, 1962–1964, 1972 (PISAS Nos 664–666/58; 745/58; 769/58; 2677/62; 1554/63; 1788/64; 1840/64; 6253/680); 10 specimens from A. brama, Břehyně Fishpond and River Vltava near Temelín, Czech Republic, 22.iv.1981, 2.vii.1987, vi.1988 (IPCAS No. C-2/1); 10 specimens from A. brama, Lac de Vouglans, France, 17.xi.1999 (IPCAS No. C-2/1); 2 specimens from Barbus barbus, River Dniester, Ukrajine, 13.vi.1961 (ZIK, not accessioned);2 specimens from Blicca bjoerkna, River Malý Dunaj near Jahodná, Slovakia, 13.v.1964 (PISAS No. 1747/64);6 specimens from B. bjoerkna, River Elbe in Střekov and Rožmberk Fishpond, Czech Republic, 1.iii.1980, 16.x.1984 (IPCAS No. C-2/2); 2 specimens from Leuciscus aspius, Donietsk, Ukraine, 16.v.1953 (ZIK No. 159-3);1 specimen (holotype) of Caryophyllaeus fuhrmanni Szidat, 1937 from Cyprinus carpio, Switzerland (MHNG-PLAT, see Mackiewicz, 1962).

(ii) Newly-collected specimens: 169 specimens from A. brama, Ballerus ballerus and Ballerus sapa, Rivers Danube, Latorica and Tisa and Zemplínska Šírava Water Reservoir, Slovakia, 2002–2011 (PISAS Nos SR 8/02; 77/04; 78/04; 79/04; 80/04; 147/04; 151/04; 182/04; 188/04; 250/04; 274/04; 82/05; 133/05 (1, 2); 410/05; 492/05; 18/06(1, 2); 48/06-1; 97/06-2; 130/06(1–4); 134/06; 136/06; 363/06(1, 2); 375/06-1; 377/06-2; 7/07; 39/07; 39/07(2-4); 41/07 (1, 2); 42/07; 43/07; 45/07A; 93/07A; 96/07(2, 3); 176/07; 1/08; 1/08-2; 25/08; 26/08(1, 2); 33/08(2–8); 37/08; 38/08; 61/08; 61/08-1; 91/08; 15/09; 15/09(1–10); 17/09; 19/09; 31/09(3, 5, 7); 33/09; 33/09-1; 39/10a; 123a/11; 142/11; 150/11; 157/11; hologenophores: SR 23/10b; 121c/11; 145c/11; 160d/11; paragenophores: SR 121(b, e)/11; 145, 145(a, b); 160/11; 160(a–c)/11); 81 specimens from A. brama, B. ballerus, B. sapa and B. bjoerkna, River Volga at Gorky, Cheboksary and Rybinsk Water Reservoirs, Russia, 2004, 2009 (PISAS Nos RU 8/09; 9 (3)/09 (1–5); 33–37/09 (2–5, 8, 9); 66/09-1; 79/09-2; 99/09, 137/09-1; 144–146/09 (3, 9); 153–157/09-4; 200/09; 206/09-1; 253–257/09(1, 2); 253(257)/09(3–5); 105–117(3, 4, 6, 11); IPCAS No. C-2/1; hologenophores: PISAS Nos RU 198/09; 201/09; paragenophores: IPCAS No. C-2/1; PISAS Nos RU 201–203 (4, 7, 9–17); 2 specimens from Pelecus cultratus, River Volga at RybinskWater Reservoir, Russia (PISAS No. RU 38/09).

Morphotype 2

(i) Specimens from museum collections: 6 specimens from Vimba vimba, River Danube near Komárno, River Hron, Slovakia, 1958, 1972 (PISAS Nos 742/58; 800/58; 6172-599; 6286-713), 5 specimens from V. vimba, River Vltava in České Budějovice, Czech Republic, x.1987 (IPCAS No. C-2/6); 5 specimens from V. vimba, Gólbasi Water Reservoir, Turkey, 2003 (see Aydoğdu et al., 2008; IPCAS No. C-2/6).

(ii) Newly-collected specimens: 25 specimens from Vimba melanops, River Arda, Bulgaria, 1.vi.2009, 2.vi.2010, 19.vi.2012 (PISAS Nos BG 11/09; 11/09-8; 14/09-2; 6/10 (1–3); 6–10/10; 12–18/10 (1, 4); 13/10-1; 28/10-1; 165/10; hologenophores: BG 13/(1, 3, 4) B12; 14/(2–5) B12; 19/2 B12; 23 B12).

Morphotype 3

(i) Specimens from museum collections: 4 specimens from Cyprinus carpio haematopterus (‘sazan’), Zelenga, Russia, 30.v.1954 (ZIK No. 1369/3); 1 specimen from ‘sazan’, Lake Kararimskoe, Russia, 19.vi.1959 (ZIK, not accessioned); 6 specimens from C. carpio, Ostrava, Czech Republic, x.1974 (IPCAS No. C-3/2); 4 specimens from C. carpio, Lake Iznik, Turkey, 21.iv.1989 (BMNH No. 1989.4.21.46–63); 1 specimen from C. carpio, Munich, Germany, xi.1994 (BMNH No. 1995.2.13.501–503).

(ii) Newly-collected specimens: 4 specimens from C. carpio, River Tisa near V. Trakany, Slovakia, iv. 2004 (hologenophore & paragenophore: TS 04/112 – SLO 22), 15.iv.2008 (PISAS Nos SR 18/08, 19/08); 3 specimens from C. carpio, River Danube at Štúrovo, Slovakia, 20.iv.2011 (PISAS No. SR 166/11).

Morphotype 4

(i) Specimens from museum collections: 7 specimens from Chondrostoma nasus, River Hron at Tlmače, Slovakia, 1958 (PISAS Nos 706, 707, 718, 720, 849, 863/58; see Žitňan,1968); 4 specimens from C. nasus, River Drau near Villach, Austria, 2000, F. Jirsa (IPCAS No. C-2/9; see Jirsa et al., 2008).

(ii) Newly-collected specimens: 47 specimens from C. nasus,River Drau at Rosegg, Austria, 28.vii.2009 (IPCAS No. C-2/9); hologenophores: AU2 i; AU2 iii; AU3; paragenophores: AU2 v; AU2 vi; 8 × AU2; 34 × AU3).

Morphotype 5

(i) Specimens from museum collections: 1 specimen from Ballerus sapa, Rákocziujfalu, Hungary, 4.vi.1965 (IPCAS No. C-2/7).

(ii) Newly-collected specimens: 5 specimens from Ballerus sapa, Rivers Latorica and Tisa, Slovakia, 2005, 2008 (PISAS Nos SR 133/05 (1, 2); 319/05; 34/08; hologenophore: SR 131/05); 2 specimens from Abramis brama, River Volga at Gorky Water Reservoir, Russia, 26.vi.2009 (PISAS No. RU 33–37/09-1).

Unidentified material from museum collections

These specimens could not be assigned to some of the morphotypes due to their poor quality or had been studied before the morphotypes of C. laticeps and C. brachycollis were recognised by Bazsalovicsová et al. (2014).

Whole-mounted specimens from Abramis brama, Egypt, Looss (BMNH 1932.5.31.269); River Colne, England, UK, 1954, W. Gertvots (BMNH 1955.7.20.74–75); from Cyprinus carpio, Austria, E. Kritscher (NMW 3008); from Squalius cephalus, Austria, E. Kritscher (NMW 3603–4); unmounted specimens from A. brama from several localities in Sweden, collected by O. Nybelin in 1927–1935 (GNHM 2685–2705; SMNH 224, 400, 401, 447); 3 contracted unmounted worms from Blicca bjoerkna,Östersjön, Sweden, O. Nybelin, 8.vii.1927 (GNHM 2684); unmounted specimens in vials designated as C. laticeps from Barbus barbus, Austria, E. Kritscher (NMW 15883); from C. carpio, Austria, E. Kritscher (NMW 15884 & 16149); from Gobio gobio, Austria, E. Kritscher (NMW 15885); from S. cephalus, Austria, E. Kritscher (NMW 15887; in fact, a mixture of Caryophyllaeus brachycollis and Caryophyllaeides fennica (Schneider, 1902), T. Scholz, unpubl. data); numerous, usually contracted and fragmented specimens designated as C. mutabilis from A. brama (ZMB 1673-E; 1674-E; 2710-E; 3700-Q; 5063-E; 7409-E); several fragments of cestodes from C. carpio (ZMB 3030-E); unmounted specimens in vials designated as C. mutabilis from Abramis brama, 1858, collected by Kollar, and Ballerus ballerus, ix.1888 (both NMW 2629); from Barbus barbus, M. Bremser (NMW 2630).

References

Aydoğdu, A., Emence, H., & Innal, D. (2008). The occurrence of helminth parasites in vimba (Vimba vimba L. 1758) of Gólbasi (Bursa) Dam Lake, Turkey. Acta Parasitologica Turcica, 32, 86–90.

Bazsalovicsová, B., Kráľová-Hromadová, I., Brabec, J., Hanzelová, V.,Oros, M., Scholz, T.(2014).Conflict between morphology and molecular data: a case of the genus Caryophyllaeus (Cestoda, Caryophyllidea), monozoic tapeworms of cyprinid fishes. Folia Parasitologica,61, 347–354.

Jirsa, F., Konecny, R., & Frank, C. (2008). The occurrence of Caryophyllaeus laticeps in the nase Chondrostoma nasus from Austrian rivers: possible anthropogenic factors. Journal of Helminthology, 82, 53–58.

Mackiewicz, J. S. (1962). Systematic position of Caryophyllaeus fuhrmanni Szidat, 1937 and Lytocestus alestesi Lynsdale, 1956 (Cestoidea: Caryophyllidea). Revue Suisse de Zoologie, 69, 729–735.

Žitňan, R. (1968). Cestoidea der Fische im Flusse Hron (ČSSR). Studia Helminthologica, 1968, 11–20.

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