1996KluwerAcademicPublishers. Printedin theNetherlands. Paranoplocephala aquatica n. sp. (Cestoda, Anopiocephalidae) from Arvicola terrestris and Ondatra ...
SystematicParasitology 34: 135-152,1996. © 1996KluwerAcademicPublishers. Printedin theNetherlands.
135
Paranoplocephala aquatica n. sp. (Cestoda, Anopiocephalidae) from Arvicola terrestris and Ondatra zibethica (Rodentia), with redescriptions and comments on related species Todor Genov, GerganaE Vasilevaand Boyko B. Georgiev Central Laboratory of General Ecology, Bulgarian Academy of Sciences, 2 Gagarin Street, 1113 Sofia, Bulgaria Acceptedfor publication5th February, 1996
Abstract
Paranoplocephala aquatica n. sp. is described from Arvicola terrestris and Ondatra zibethica (Rodentia, Cricetidae) in Bulgaria. The new species is characterised by a band-like strobila, a uterus forming a free reticulate structure in the early stages of development, numerous testes (approximately 92) situated mainly aporally to the ovary in both the median and the aporal lateral fields, few testes positioned anterior to the ovary and genital ducts, the prominent asymmetrical situation of the female organs, the length of the vagina c. 0.65-0.68 of the length of the cirrus-sac, and the external seminal vesicle covered by a cellular sleeve. The new species is distinguished from P. ondatrae, P. macrocephala, P. dasymidis and P. sciuri. The specimens from O. zibethica reported as P. ondatrae by Tenora & Murai (1980) and as Aprostatandrya macrocephala by Spasskii et al. (1951) are believed to belong to P. aquatica. The type-series ofP. ondatrae and P. macrocephala are redescribed and figured; metric data and an illustration of the holotype ofP. sciuri are presented. The genus Paranoplocephala sensu Tenora et al. (1986) is regarded as a heterogeneous group because of the two patterns of uterine development in the species studied. Taxonomic criteria used for distinguishing the genera Andrya and Paranoplocephala, and some criteria applicable at the species level, are discussed. Introduction
Previous studies (Genov, 1964, 1984) on the helminth parasites of aquatic voles in the Lake of Srebama, NE Bulgaria, revealed the presence of cestodes of the genus Paranoplocephala Ltihe, 1910 in cricetid rodents Ondatra zibethica (L.) and Arvicola terrestris (L.). These cestodes were reported as Aprostatandrya macrocephala (Douthitt, 1915) by Genov (1964) and as Paranoplocephala blanchardi (Moniez, 1891) by Genov (1984). Since these identifications do not correspond well with recent knowledge of the host specificity and geographical distribution of Paranoplocephala spp. (see Rausch, 1976; Tenora & Mural, 1980; Tenora et al., 1985, 1986), an attempt to re-examine them was made. However, the specimens available were in a contracted state and did not permit adequate study of their morphology. New specimens were, therefore, collected from the same locality. The identification of these cestodes resulted in the description of a new species
and redescriptions of type-specimens of several already known species of Paranoplocephala.
Materials and methods
The specimens of the new species, collected by T. Genov and B.B. Georgiev from the small intestines of their hosts, were relaxed in tap-water and fixed in 70% ethanol. They were stained in iron acetocarmine, dehydrated in alcohol, cleared in eugenol and mounted in Canada balsam. Specimens of P. ondatrae (Rausch, 1948) (holotype), P. sciuri (Rausch, 1947) (holotype), P. macrocephala (Douthitt, 1915) (syntypes) and cestodes from O. zibethica from Central Europe determined as P. ondatrae by Tenora & Murai 1980) were used as comparative material. Details of the fixation and preparation methods are given individually for each species. The abbreviations for the collections in which the specimens were deposited are as follows: NHM, Par-
136 asitic Worms Division, The Natural History Museurn, London; HNHM, Parasitology Collection, Department of Zoology, Hungarian Natural History Museum, Budapest; USNPC, US National Parasite Collection, Beltsville; and TG, the Collection of T. Genov, Bulgarian Academy of Sciences, Sofia. The measurements of the cirrus-sac, seminal vesicles, vagina and seminal receptacle were taken from mature and post-mature proglottides. Two indices were used: (1) Ia (index of asymmetryof the female organs, see Sato et al., 1993), the ratio of the distance between the poral proglottis margin and the centre of the vitellarium to the proglottis width; and (2) Iv (describing the relative length of the vagina), the ratio of the length of the vagina to the length of the cirrus-sac. The metric and meristic data are given as the range, the mean in parentheses and the number of measurements or counts taken (n). The measurements are given in micrometres unless where otherwise stated.
Paranoplocephala aquatica n. sp. Synonyms: Paranoplocephala ondatrae of Tenora & Murai (1980); Aprostatandrya macrocephala of Spasskii et al. (1951). Specimens studied Holotype: NHM 1995.8.16.1, Arvicola terrestris (L.), small intestine, Srebarna, 27.04.1984 (coll. no. 88822); one whole pregravid specimen, 1 slide. Paratypes: from A. terrestris: NHM 1995.8.16.2-3, with the same data as the holotype; one whole mature specimen (1 slide, coll. no. 8882-10) and fragments (including gravid ones) of several specimens (1 slide, (coll. no. 8882-9). HNHM 67368/1,2, with the same data as the holotype; 3 specimens, 2 slides. TG nos 8882-1 (5 premature specimens), 8882-4 (1 mature specimen), 8882-5 (2 premature specimens), 8882-6 (fragments), 8882-8 (fragment), 8882-11 (numerous fragments, including gravid ones), and 8882-12 (whole mature specimen); 7 slides, with the same data as the holotype. from O. zibethica (L.): NHM 1995.8.16.4, Srebarha, 28.04.1984 (coll. no. 8904), entire gravid specimen (fragmented), 1 slide. TG 10141-1, Srebama, 19.04.1985, entire mature specimen, 1 slide. Other specimens: HNHM Nos 479, 483, 484 and 487, small intestines, O. zibethica, Ceske Budejovice (Czech Republic), 10.1955, coll. Dr E Tenora; 4 slides (2 with whole specimens and 2 with fragments); fixed in 5% formalin,
stained in carmine (? hydrochloric carmine), mounted in Canada balsam. HNHM No. 3236, small intestine, O. zibethica, Orgovany (Hungary), 11.09.1971, coU. Dr I. Matskasi; 1 slide with whole-mount (stained in carmine) and 1 slide with frontal sections ofpostmature proglottides (stained in haematoxylin-eosin), mounted in Canada balsam.
Description Strobila band-like, with maximum width at gravid or pregravid proglottides. Scolex (Figures 1,2) wider than neck, clearly distinct from it; apical end rounded. Suckers muscular, orifices directed anteriorly. Neck long, narrowest just posterior to scolex. Proglottides (Figures 3--7) craspedote, wider than long in all stages of their development; length/width ratio of premature proglottides 1:2.6--4.3 (1:3.3, n = 10), of mature proglottides 1:3.1-4.4 (1:3.7, n = 15), of postmature proglottides 1:3.7-4.8 (1:4.3, n = 5), of gravid proglottides 1:1.92.4 (1:2.1, n = 10). Genital atria (Figure 8) infimdibular, simple, surrounded by intensely stained tissue; opening at about middle of lateral proglottis margin. Genital pores alternating, mainly in large series, e. g., ... 29,7,8, 1,41, 1,6,8, 17,2,9,3,29,7 ... (specimen fromA, terrestris); ... 35, 7, 15, 55 ... 69, 91 (specimen from O. zibethica). Ventral osmoregulatory canals with transverse anastomosis in each proglottis. Dorsal osmoregulatorycanals simple; transverse anastomoses not observed. Genital ducts dorsal to poral osmoregulatorycanals. Testes numerous, in several layers except dorsal to aporal osmoregulatory canal where single layer only present; most testes (Figures 3-5) situated aporally to female glands both in median field and in aporal lateral field; few testes situated anteriorly and anteroporally to female glands, often extending into poral lateral field (Figure 3); individual testes may overlap aporal and anterior lobes of ovary. Cirrus-sac (Figure 8) pyriform, thick-walled, almost perpendicular to longitudinal strobilar axis; overlaps or just crosses poral osmoregulatory canals. Armature consisting of small spines presents in ductus cirri. Intensely staining cells surround duetus cirri. Large internal seminal vesicle present. External seminal vesicle elongate, curved or forming 1-2 loops; covered by layer of cells (not intensely stained) (Figure 8). Vagina (Figure 8) opens posteriorly to male pore; surrounded by thick, cellular sleeve; always shorter than cirrus-sac. Seminal receptacle (Figures 3-5) extends from slightly poral of osmoregulatory canals,
137
3
4
i Figures 1-5. Paranoplocephala aquatica n. sp. 1. Scolex of a specimen from O. zibethica. 2. Scolex of a specimen from A. terrestris. 3, 4. Mature proglottides of specimens from O. zibethica. 5. Mature proglottis of a specimen from A. terrestris. Scale-bars: 1,2, 200/zm; 3-5, 250 #m.
138
~:,':'j:'!',l~'I~:,:)~'~?!;~~:~!'',~,~'" Figures 6-8. Paranoplocephala aquatica n. sp. 6. Reticulate uterus in a well-developed mature proglottis (testes omitted), ventral view. 7. Gravid proglottis, ventral view. 8. Terminalgenital ducts in matureproglottis. Scale-bars: 6, 200 #m; 7, 500/zm; 8, 100 #m.
dorsal to poral lobes o f ovary, to anterior to poml lobe o f vitellarium; fusiform to elliptical. Mehlis' gland large, globular, anterior to vitellarium. Vitellarium and ovary situated porally. Vitellarium (Figures 3-5) asym-
metrical, more or less reniform, lobed. Ovary fanshaped, highly lobed; anterior and lateral lobes larger than posterior lobes.
139 Uterus initially reticular (Figure 6), situated both in median field and in lateral fields, ventral to testes and female glands; later spongiose, with many external and internal diverticula (Figure 7). Eggs globular, thinwalled, with pyriform apparatus. Measurements See Table I. Measurements not included in Table I: diameter of ventral osmoregulatory canals 54-81 (69, n = 10); diameter of dorsal osmoregulatory canals 1831 (26, n = 10). Remarks Previously, cestodes of aquatic voles, Arvicola terrestris, A. sapidus (Miller) and Ondatra zibethica, from the Palaearctic Region have been identified as Paranoplocephala macrocephala (Douthitt, 1915) (see e.g. Spasskii et al., 1951; Tenora, 1956; Genov, 1964; Ryzhikov et al., 1978), P. omphalodes (Hermann, 1783) (see e.g. Akhumyan, 1956; Ryzhikov et al., 1978; Feliu et al., 1992), P. caucasica (Kirshenblat, 1938) (see Ryzhikov et al., 1978), P. ondatrae (Rausch, 1948) (see Tenora & Murai, 1980; Tenora et al., 1985), P. blanchardi (Moniez, 1891) (see Genov, 1984) and P. gracilis Tenora & Mumi, 1980 (see Schuster, 1987; Feliu et al., 1992). However, these determinations have been based on comparisons with published descriptions of the above-mentioned species, without a relevant comparative study of type-specimens. P. aquatica n. sp. will not be compared in detail with P. omphalodes, P. caucasica and P. gracilis, since these species are characterised by a considerably smaller number of testes and a different pattern of their arrangement. P. omphalodes, parasitic in a wide range of voles in the Holarctic, has been characterised by approximately 45 testes (the lectotype, Tenora & Murai, 1980), 35-51 (Tenora & Murai, 1980) or 3642 (Genov, 1984). P. caucasica, originally described from Microtus socialis Pallas in Georgia, has 26-34 testes (Kirshenblat, 1938). The testes ofP. omphalodes and P. caucasica are situated aporally to the ovary and never anteriorly to the female glands. The number of testes in P. gracilis is 45-55 (Tenora & Murai, 1980) or 41-46 (Genov, 1984); only a few testes may pass beyond the aporal osmoregulatory canals (Tenora & Murai, 1980; Tenora et al., 1985). The new species, however, needs to be distinguished from P. macrocephala and P. ondatrae. The former species has been believed to show a great vari-
ability of the number of testes, i.e. 24--106 (Rausch & Schiller, 1949). The latter has been reported to possess 75-95 (Rausch, 1948) or 70-90 testes (Tenora & Murai, 1980). Regarding the species described outside the Palaearetie, comparisons are needed with those belonging to the morphological group chamcterised by a vagina longer than half the length of the cirrus-sac, testes in both aporal and poral halves of mature segments, some of them 'across or beyond' the ventral canals, and an elongate seminal receptacle (Tenora et al., 1986). Among the members of this group, only P. macrocephala, P. ondatrae, P. dasymidis (Hunkeler, 1972) and P. sciuri (Rausch, 1947) have been reported with a number of testes near that ofP. aquatica. Of the species mentioned, P. ondatrae was originally recorded from an aquatic vole (Rausch, 1948). It was described, as a member of the genus Andrya Railliet, 1893 on the basis of one specimen found in the course of the examination of 200 muskrats in the North Central USA. Rausch (1948) believed that this cestode might be either very local in its distribution or an accidental parasite of the muskrat. Rausch & Schiller (1949) recognised A. ondatrae, together with other Holarctic species, as synonyms of A. macrocephala. However, when analysing data on the host specificity and the geographical range of P. macrocephala, Rausch (1976) supposed that it represented a complex of species. In accordance with this conclusion, Tenora & Mural (1980) validated A. ondatrae and placed it in the genus Paranoplocephala. They gave a description of specimens from O. zibethica from Central Europe (Czech Republic and Hungary) identified as P. ondatrae. Tenora et al. (1986) also recognised P. ondatrae as a valid species. In order to identify the specimens from A. terrestris and O. zibethica from Bulgaria, we re-examined the holotype of P. ondatrae (see below). Our cestodes differ considerably from the North-American material in several characters of major taxonomic significance at the species level. The female glands are disposed porally in Bulgarian specimens, i.e., IA is c. 0.33-0.37, whilst in the type ofP. ondatrae the female glands are central (IA averages 0.48). Another important species character is the length of the vagina related to the length of the cirrus-sac. In Bulgarian cestodes Iv averages 0.65-0.68 (i.e. the length of the vagina is more than half that of the cirrus-sac) whilst the vagina ofP. ondatrae is extremely short (Iv averages 0.23). The pattern of the testes distribution is also different in the forms compared. In P. ondatrae, there are many testes anterior to the female glands and only occasional
140
Table1. Metric and meristicdata for Paranoplocephalaaquatican. sp. Host Locality Source
Strobila: length (ram) width (ram) Seolex: diameter Suckers: diameter Neck: length ( m m ) min. width Testes: number Cirrus-sac: length width Internalseminalvesicle: length width External seminalvesicle: length width
IA Vagina: length width of sleeve width of lumen Seminalreceptacle: length width
IvEggs: diameter Oncospheres: diameter
,4rvicola terrestris
Ondatrazibethica
Ondatrazibethica
O. zibethica
Bulgaria Present study Range Mean n
Bulgaria Present study Range Mean n
Czech Republic Present study Range Mean n
Russia Spasskii et al. 1951 Range
3.24-4.27 505-678 179-277 1.25-1.27 284-481 96-128
70-100 3.5 4004500 200-300 80-100
178 1 113 1.86-2.65 2.30 5 2.14 407-619 475 12 562 152-237 187 52 179-196 0.88-1.491.14 12 0.94 219-367 297 13 215 76-110 92 16 78-115
189 93
1 1 1 4 1 1 14
234 109
2 2 8 2 2 10
157-201 67-89
184 77
12 174-228 208 12 63-103 85
12 205-299 254 12 98-121 107
14 160-300 14 90-100
58-98 49-67
78 54
12
12 67-130 40~9
12 72-161 12 63-107
14 14
93 60
119 87
-
-
93-147 125 17-31 22 0.30-0.38 0.33
11 143-232 180 11 27-54 38 10 0.354).40 0.37
12 215-349 282 12 27-56 41 10 0.32-0.37 0.34
12 12 10
103-156 45-76 14-27
120 59 20
12 134-170 153 12 49-103 72 12 22-39 27
12 121-241 168 12 71-121 91 12 18-31 25
14 200 14 14 -
215-339 76-143 0.53-0.79 38-41 9-12
262 105 0.65 39 11
12 12 12 15 15
12 12 12 15 15
14 14 14 -
233-348 63-143 0.614).82 42-50 11-14
testes overlap the ventral osmoregulatory canals; testes never pass beyond the aporal dorsal osmoregulatory canals. In our material, most o f the testes are situated aporally to the female glands, both in the median field and in the aporal lateral field, and only a few testes are present anterior to the ovary and the genital ducts. Further comparisons o f the genital ducts exhibit differences: in the structure o f the external seminal vesicle (surrounded b y a sleeve o f large ceils in our material compared with no cellular sleeve but walls built up of large squamous cells in P. ondatrae); in the shape of the seminal receptacle (from fusiform to elliptical in our specimens compared with consisting of a tubular poral region and an elongate-ovoid aporal part in P. ondatrae); in a constant posterior position of the vaginal orifice in relation to the male pore in the specimens
289 91 0.68 46 13
573-745 646 112-286 193 0.53-0.82 0.66 -
-
700 30-40 12
from Bulgaria compared with a variable position in P. ondatrae (see redeseription below); and in a different position of the genital pore (about the middle of the lateral proglottis margin in P. aquatica compared with in the posterior 1/5-1/4 in P. ondatrae), Therefore, there are no grounds for identifying our specimens as
P. ondatrae. Another species name very often used for the cestodes o f the aquatic voles in the Palaearctic is P. macrocephala. Originally, this species was described on the basis of specimens from Geomys bursarius Shaw (Geomyidae) in North America (Douthitt, 1915). Later, cestodes of various rodent hosts (species o f Geomyidae, Muridae and Cricetidae, including both Cricetinae and Microtinae) from North America and Eurasia were identified as P. macrocephala (see Rausch &
141
'
'
\9
Figures9-10. Paranoplocephala aquatican. sp., matureproglottidesof specimensfromO. zibethica fromthe CzechRepublic(=P. ondatrae of Tenora& Murai, 1980).Scale-bar:250 #m. Schiller, 1949; Ryzhikov et al., 1978). We share the opinion of Rausch (1976) that 'the species has been characterised within limits so broad as to prevent discrimination between the variants and macrocephalalike species'. Therefore, in order to have a reliable basis upon which judge the use of the name 'P. macrocephala' for Palaearctic cestodes, we re-examined the syntypes of this species. P. aquatica n. sp. differs from the type-series of P. macrocephala mainly in the number and the distribution of the testes. Whilst in P. aquatica the number of testes number averages 92-93, in P. macrocephala their number is approximately half, averaging 48. In P. macrocephala, they form a compact group extending from the aporal lobes of the ovary to the aporal ventral osmoregulatory canals, often overlapping them; there are no testes both anterior to the ovary and in the aporal lateral field. The pattern of testes distribution in P. aquatica is quite different (see above). In addition, the genital pores ofP. macrocephala are posterior compared with the median position of the pores in P. aquatica. P. aquatica differs from P. sciuri in the pattern of distribution of the testes. Whilst in the former species the testes are situated anteriorly to the ovary and the genital ducts are rather few, in the latter species about
one third to half of the testes are anterior and anteroporal to the ovary. The asymmetrical location of the female organs ofP. sciuri is very slight (/it is 0.430.50, av. 0.46) compared with the prominent asymmetry in P. aquatica. The genital pore in P. sciuri is posterior. Although the structure of the mature proglottis (especially the pattern of the testes distribution) of P. dasymidis resembles that of P. aquatica, we did not examine specimens of this species. The reason for this is that P. dasymidis has a rather wedge-shaped strobila: 10-20 mm long and 4 mm wide (Hunkeler, 1972; 1974) and clearly differs in this character from the new species. All these comparisons provide sufficient grounds to consider that our material from A. terrestris and O. zibethica belongs to a new species. Tenora & Murai (1980) reported cestodes from O. zibethica from Central Europe as P. ondatrae. Their specimens were re-examined during the course of the present study. The morphology of these cestodes (see Table I; Figures 9,10) differs from the holotype of P. ondatrae by all the differentiating characters mentioned in the above comparison with P. aquatica. They resemble closely the type-specimens of P. aquatica, apart from some metric characters: the width of the
142
1
I
I
I
13
Figures 11-14. Paranoploccphalaondatrae (Rausch, 1948). 11, 12. Mature proglottides showing variability of the distribution of the testes, uterus omitted. 13. Early stage of uterine development (in the same proglottis shown in Figure 12). 14. Terminal genital ducts. Scale-bars: 11-13,250/~m; 14, 100/tm.
143 strobila and the sizes of the cirrus-sac, seminal vesicles and seminal receptacle (Table I). However, IA, 1V, the number and arrangement of the testes, and the position of the genital pores are very similar. The metric differences observed may be due to the fixation under pressure, which was probably applied to the specimens of Tenora & Murai (1980). Therefore, with some reservation, we ascribe the specimens from the Czech Republic and Hungary to P aquatica. Spasskii et al. (1951) reported cestodes from O. zibethica from Arkhangelskaya Oblast' (northern European Russia) and Kurganskaya Oblast' (Siberia) as Aprostatandrya macrocephala. They gave a detailed description of their specimens, unfortunately unillustrated. The metric data presented by them (Table I) correspond well to those of our material and especially those from the Czech specimens. The description of the arrangement of the testes in the Russian material resembles that in the Bulgarian and the Czech cestodes: 'Testes numerous, not less than 80-100. They are situated in three or four layers aporally and anteriorly to the complex of the female genital glands. Part of the testes usually pass dorsally to the aporal excretory canal into the lateral field of the proglottis. A small number of testes occur porally to the ovary, anterior to the vagina'. In addition, the female genital glands were described as porally disposed. As far as we can judge on the basis of the metric data, the length of the vagina is approximately two-thirds of the length of the cirrus-sac. All these data suggest that the cestodes of Spasskii et al. (1951) also belong to P. aquatica.
Paranoplocephala ondatrae (Rausch, 1948) Synonyms: Andrya ondatrae Rausch, 1948; Aprostatandrya ondatrae (Rausch, 1948) Spasskii, 1951. Specimen studied USNPC 46326, holotype, from small intestine of Ondatra zibethica, 20 November, 1944, upper Walnut Creek, Morrow County, Ohio, coU. R.L. Rausch; fixed in 10% formalin, stained in Semichon's acetic carmine and mounted in Canada balsam. Redescription Strobila band-like, consisting of 369 proglottides; maximum width in gravid proglottides. Seolex wider than neck, with rounded apical end and maximum diameter at level of suckers. Suckers muscular, oval, opening almost laterally. Neck long, narrowest at about
its middle. Proglottides (Figures 11,12) craspedote, wider than long at all stages of their development; length/width ratio of premature proglottides 1:3.5-10.9 (1:6.8, n = 10), mature proglottides 1:2.7-4.9 (1:3.6, n = 10), postmature proglottides 1:2.9-3.7 (1:3.3, n = 9), gravid proglottides 1:2.3-3.2 (1:2.7, n = 5). Genital atria (Figure 14) simple, tubular, surrounded by intensely staining tissue, opening in posterior 1/5-1/4 of lateral proglottis margin. Genital pores irregularly alternating in long series (e.g. . . . 36, 83, 46, 56 ... ). Ventral osmoregulatory canals with transverse anastomoses along posterior margins of proglottides. Dorsal osmoregulatorycanals without transverse anastomoses. Genital ducts dorsal to poral osmoregulatory canals. Testes (Figures 11,12)numerous, situated in several layers; most of testes in median field, aporal and anterior to ovary; some of them overlapping anterior and lateral ovarian lobes; few testes antero-porally to ovary; few testes overlap aporal ventral osmoregulatory canal in single layer; individual testes may overlap poral ventral osmoregulatory canal; testes never pass beyond dorsal osmoregulatory canals. Cirrus-sac (Figure 14) pyriform, widely rounded aporally; thickwalled, with moderately developed musculature; perpendicular to longitudinal strobilar axis, situated in lateral field, sometimes reaching, overlapping or just crossing dorsal osmoregulatory canal; may reach ventral osmoregulatory canal; never passing into median field. Intensely staining cells surround ductus cirri. Internal seminal vesicle large, ovoid, occupies more than half cirrus-sac; oval. External seminal vesicle (Figure 14) highly elongate; curved, makes one or 2 loops; wall composed of large intensely stained squamous cells. Evaginated cirrus unarmed, almost claviform. Vagina (Figure 14) usually opening ventrally or postero-ventrally to male pore and passing posteriorly to cirrus-sac; in some proglottides (24%), vaginal opening antero-ventral and vagina passing anteriorly to cirrus-sac; vagina considerably shorter than cirrussac; vaginal lumen tubular, very narrow; thick cellular sleeve comprises vaginal lumen and poral end of seminal receptacle. Seminal receptacle highly elongate; poral half (from vagina to level of ventral osmoregulatory canal) tubular; aporal part elongate-ovoid; wall composed of large intensely stained squamous cells. Mehlis' gland large, globular. Vitellarium (Figures 11,12) situated centrally or almost centrally; asymmetrical, lobate, poral part parallel to posterior proglottis margin; aporal part directed antero-porally. Ovary fan-
144
.5 J ,
f"~
.--
'~ \ 1 6
17
....... -\
18 Figures 15-18. Paranoplocephala macrocephala (Douthitt, 1915), proglottides. 15. Mature proglottis, dorsal view; note the early stage of uterine development. 16. Late mature proglottis, ventral view. 17. Postrnature proglottis. 18. Pregravid proglottis. Scale-bars: 200/zm.
145 shaped, with long digitiform lobes; anterior and lateral lobes longer than posterior lobes. Uterine duct visible in all mature proglottides, directed antero-aporally, situated dorsally to ovary and connected with uterine reticulum at level of tips of anterior ovarian lobes. Uterus initially visible (Figure 13) in well-developed mature proglottides (204th proglottis) as fine reticulum covering entire median field and half of lateral fields ventrally; anteriorly, reaching almost to anterior proglottis margin; posteriorly, reaching level of Mehlis' gland. First eggs appear in uterus in 244th245th proglottis, initially occupying median part of uterus and anterior portions of uterus in lateral fields. With increasing of number and size of eggs (258th proglottis), reticular structure of uterus disappears, external margins become slightly lobate and numerous internal compartments appear. Uterus situated ventrally to all other internal organs, but does not displace testes during its development. Gravid uterus occupies almost entire proglottis. Eggs sub-cylindrical, with concave bases; oncospheres round; pyriform apparatus present.
Measurements See Table II. Measurements not included in Table II: diameter of ventral osmoregulatory canals 116-157 (140, n = 10); diameter of dorsal osmoregulatory canals 13-22 (17, n = 10); cirrus: length 45-58 (51, n = 10), maximum width 22-27 (25, n = 10); minimum width 13-18 (15, n = 10).
Remarks The present re-examination of the holotype ofP. ondatrae confirms the original description (Rausch, 1948), including the metric data (see Table II). There are, however, some differences concerning the general dimensions of the strobila and the measurements of the seminal receptacle. The latter is probably due to the different interpretations of the structure of the female genital ducts. Rausch (1948) probably regarded as the seminal receptacle only the elongate-ovoid part of the organ situated in the median field. The present redescription provides additional information to the original data with regard to the pattern of uterine development, the relative length of the vagina in comparison to the cirrussac, the structure of the genital atrium and the degree of the asymmetry of the female organs.
Paranoplocephalamacrocephala(Douthitt, 1915) Synonyms: Andrya macrocephala Douthitt, 1915; Aprostatandrya macrocephala (Douthitt, 1915) Spasskii, 1951.
Specimens studied USNPC 49517, syntypes ('cotypes'), from small intestine of Geomys bursarius, 8 August, 1911, Brainerd, Minnesota, coll. H. Douthitt; 3 specimens preserved in 70% ethanol; 2 of them bleached in Meyer's chlorine, stained in iron acetocarmine, dehydrated in alcohol series, cleared in eugenol and mounted in Canada balsam as whole-mounts (4 slides) or sections of mature and postmature proglottides made with razor blade by hand, i.e. transverse sections (2 slides) or longitudinal sections (2 slides).
Redescription Strobila band-like, consisting of 329-350 proglottides, with maximum width at postmature proglottides. Scolex wider than neck, clearly distinct from it; apical end rounded. Suckers muscular, ovoid, with their orifices directed anteriorly. Neck long, narrowest just posterior to scolex. Proglottides (Figures 15-18) craspedote, most of them wider than long; length/width ratio of premature proglottides 1:6.0-9.6 (1:7.2, n = 10), mature proglottides 1:5.0-6.0 (1:5.5, n = 10), postmamre proglottides 1:5.3--6.5 (1:5.9, n = 6), pregravid proglottides 1:0.7-2.4 (1:1.6, n = 8). Genital atrium infundibular, muscular, surrounded by intensely staining cells; opening in posterior third of lateral proglottis margin. Genital pores alternating in large series (... 21, 19, 2, 49, 7, 1, 2, 3, 4, 9, 6, 42, 5 ...). Genital atrium may form prominent genital papilla. Ventral osmoregulatory canals strongly developed, with transverse anastomosis in each proglottis. Dorsal osmoregulatory canals simple; transverse anastomoses not observed. Genital ducts dorsal to poral osmoregulatory canals. Testes (Figure 15) situated in several layers aporally to female glands in median field; few testes overlap aporal osmoregulatory canals but never pass into lateral field; one or 2 testes overlap aporal ovarian lobes; no testes observed anterior to ovary. Cirrus-sac (Figure 19) ovoid, slightly elongate, thick-walled, overlaps or just crosses poral osmoregulatory canals. Ductus cirri provided with armament consisting of small spines, surrounded by glandular cells. Internal seminal vesicle (Figure 19) small, situated in aporal third of cirrus-sac.
146 TableII. Metric and meristic data f r o m the holotype (Rausch, 1948) Source
ofParanoplocephala ondatrae
Rausch (1948)
Present study
Range
Mean
Range
Mean
length ( m m )
155
-
122
-
1
w i d t h (mm)
3
-
2.58
-
1
Scolex: diameter
682
-
665
-
1
Suckers: diameter
250
-
237-250
246
4 1
n
Strobila:
Neck: length ( m m )
0.7
-
0.7
-
min. width
-
-
241
-
75-95
83
80-95
86
Testes: n u m b e r
1 15
Cirrus-sac: length
213--224
-
210-228
221
12
width
113--122
-
113--125
117
12
length
100--156
-
139-160
152
12
width
-
-
100-121
105
12
length
-
-
358-447
400
10
width
-
-
72-112
93
10
--
--
0.46-0.50
0.48
12
Intemal seminal vesicle:
External seminal vesicle:
IA: Vagina: length
-
-
45-58
51
12
width o f sleeve
-
-
40-49
43
12
length
213--340
278
626-693
669
10
width
99-127
118
112-215
143
10
Iv
-
-
0.20-0.26
0.23
12
Eggs: diameter
33-40
36
34-38
36
15
Oncospheres: diameter
-
-
9-13
12
15
Seminal receptacle:
Figure 19. Paranoplocephalamacrocephala (Douthitt, 1915), transverse section at the level o f the terminal genital ducts, detail. Scale-bar: 100 ~m.
147 External seminal vesicle highly elongate, forming one or 2 loops. Vagina (Figure 19) conical, always shorter than cirrus-sac, opening posteriorly to male pore; poral part thick-walled, surrounded by sleeve of large glandular cells; internal surface of walls with lining of free triches; aporal part of vagina tubular, thin-walled, covered with small cells. Seminal receptacle highly elongate, dorsal to poral lobes of ovary; its aporal part oval. Mehlis' gland globular. Vitellarium and ovary situated porally (Figure 15). Vitellarium asymmetrical, more or less reniform, lobed. Ovary fan-shaped, highly lobulate. Initial stage of uterine development not observed. In well-developed mature proglottides (Figure 15) uterus seen as system of numerous narrow empty canals extending mainly transversely and connected with few longitudinal and oblique anastomoses, assuming crude, bi-winged, reticulate structure; lateral extremities overlapping or extending slightly beyond osmoregulatory canals, wider than median part; uterus situated ventrally to all internal organs in anterior half of proglottis. With further development (Figure 16), when eggs appear in uterus, they occupy mainly median part and most anterior portions of lateral wings; median part starts to produce anterior and posterior sacculations; later on, median part increases in size, ventrally to testes and vestigial ovary, and numerous fenestrations appear (Figure 17). In pregravid proglottides (Figure 18), uterus occupies both median field and half of lateral fields. Fully-developed uterus and eggs not observed.
Measurements See Table III. Measurements not included in Table III: diameter of ventral osmoregulatory canals 91250 (162, n = 10); diameter of dorsal osmoregulatory canals 14-23 (17, n = 10). Remarks The present re-examination confirms most of the characters described originally (Douthitt, 1915). There is an important difference in the pattern of testes distribution. We did not observe testes situated anteriorly to the ovary in the syntypes studied, as described and illustrated by Douthitt (1915, figure 9).
Paranoplocephalasciuri (Rausch, 1947) Synonyms: Andrya sciuri Rausch, 1947; Aprostatandrya sciuri (Rausch, 1947)Spasskii, 1951.
Specimen studied USNPC 45775, one slide containing anterior part of strobila (last proglottides postmature) from holotype (one of two slides containing an entire specimen and marked originally as 'type', see Rausch, 1947), from small intestine of Glaucomys sabrinus Shaw, Millston, Jackson County, Wisconsin, 22-23 February, 1947, coll. R. L. Rausch; stained in carmine, mounted in Canada balsam. Remarks Since most of the present observations confirm the original description (Rausch, 1947), a complete redescription is not prepared for the present publication. Some metric data are given in Table IV. The structure of the mature proglottis is presented in Figure 20. The quality of the available whole mount does not permit a detailed description of the early stages of the uterine development.
Discussion The species described above belong to a cestode group parasitising mainly Holaretic rodents and consisting of at least 25 species (Tenora et al., 1986). This group has quite a confused taxonomic history at both generic and specific levels. Unfortunately, adequate contemporary descriptions of the species are few (Rausch, 1976; Tenora et al., 1985) and this restricts a well-grounded classification. Three generic names have been widely used for the species of this group: Andrya RaiUiet, 1893; Paranoplocephala Ltilae, 1910; and Aprostatandrya Kirshenblat, 1938. Rausch (1976) considered that the external seminal vesicle in Andrya rhopalocephala (Riehm, 1981) (type-species of Andrya) and A. cuniculi (Blanchard, 1891) (two species from the Leporidae), interpreted by the early authors as 'pedunculated prostate glands', did not differ fundamentally from those in cestodes from rodents. He believed that, if any significant difference between Andrya and the other two genera exists, it could only be in the character of the uterus; if the pattern of the uterine development in the type-species of Andrya does not differ from that in P. omphalodes and A. macrocephala, the genera Paranoplocephala and Aprostatandrya would become synonyms of Andrya (see Rausch, 1976). Tenora & Murai (1978) confirmed that the 'prostate gland' of A. rhopalocephala is an external semi-
148
Table IlL Metric and meristic data from the syntypes of Paranoplocephala macrocephala (Douthitt, 1915). Source
Douthitt( 1915)
Present study
Range
Range
Mean
n
Strobila: length (mm)
100-200
90
-
1
width (mm)
1.5
2
-
1
2
Scolex: length
700-950
516-573
-
width
600-800
711-722
-
2
300
358-402
389
8
length (mm)
1.5
-
-
min. width
20~600
505-516
-
43-57
42-57
48
12
Suckers: diameter Neck:
Testes: number
2
Cirrus-sac: length
155
152-170
161
12
width
35-75
54--63
57
12
length
-
47-72
54
12
width
-
39-47
44
12
Internal seminal vesicle:
External seminal vesicle: length
-
180-286
246
4
width
-
22-27
24
4
--
0.36-0.39
0.38
8
IA: Vagina: length
-
90-107
102
width of sleeve
-
20-22
21
12
7
length
-
349-380
367
5
width
-
67-116
96
5
-
0.71-0.88
0.80
7
Seminal receptacle:
Iv
Figure 20. Paranoplocephalasciuri (Rausch, 1947), mature proglottis. Scale-bar: 250 #m.
149 TableIV. Metric and meristic data for Paranoplocephalasciuri (Rausch, 1947) Source
Strobila: length (mm) width (mm) Scolex: diameter Suckers: diameter Neck: length (ram)
Rausch (1947) Range
Cirrus-sac: length width Internal seminal vesicle:
n
170 2 380
380
-
1
150
148--152
151
3
356
-
1
182
-
1
93-109
100
8
rain. width Testes: number
Presentstudy Range Mean
100-110 200
170-187
179
5
85
76--81
79
5
length
76
-
2
width
54
-
2
External seminal vesicle:
length
157-179
-
2
width
54-67
-
2
0.434).50
0.46
Ia Vagina: length width of sleeve Seminal receptacle: length width Iv Eggs: diameter
10
125-134
130
5
45-54
50
5
420
340-492
407
3
180
81-107
92
3
0.70-0.75
0.73
5
52-56
nal vesicle covered with glandular cells; they also questioned the taxonomic value of this structure at the generic level. With regard to the uterus, it was described as 'reticulate already in earliest discemable stage of development and situated anteriorly to the ovary' (Tenora & Murai, 1978). The glandular covering of the external seminal vesicle was indirectly considered as a character of minor taxonomic value at the generic level by Rausch (1980). He did not mention this structure in the amended diagnosis of the genus Diandrya Darrah, 1930. Tenora et al. (1984, 1986) found substantial differences in the early stages of the uterine development in the type-species of Andrya and Paranoplocephala. In Andrya, they reported that the uterus forms a wellexpressed reticulate structure situated ventrally in the mature proglottides (evidently, even before being filled with eggs); in Paranoplocephala, they believed that the uterus appears anteriorly as a transversely elon-
gate aggregation which, with its further development, forms 'an organ with network-like structure with uterine diverticula' (Tenora et al., 1986). Since these differences were not illustrated, we here present figures of mature proglottides showing the early stages of uterine development in A. rhopalocephala and P. omphalodes (Figures 21,22). These illustrations were made from very well-stained mounts of the two species which had been used in the comparative study of uterine development (Tenora et al., 1984, 1986), kindly donated by Dr E. Murai (Hungarian Natural History Museum, Budapest). Tenora et al. (1986) retained inAndrya only the two species from the Leporidae. They mentioned, however, that a similar structure of the uterus had been observed in some cestodes from rodents. They placed all the species from rodents in the genus Paranoplocephala (syn. Aprostatandrya). Beveridge (1994) recognised three general patterns of uterine development within the subfamily Anoplo-
150
S
( I
21
2 Figures 21-22. Early stages of uterine developmentin mature proglottidesof the type-speciesof the genera Andrya Railliet, 1883 and Paranoplocephala Lfihe, 1910.21. A. rhopalocephala (Pdehm,1881) fromLepuseuropaeusPallas, Hort(Hungary),26 April 1973, coil E. Murai. 22. P. omphalodes(Hermann,1783)fromMicrotusarvalisPallas,Buk (Hungary),19 September 1973,coll. F. Meszaros.Scale-bar: 200 #m. cephalinae. The first one does not occur in the species discussed in this paper. The second pattern corresponds to that described earlier (Rausch, 1976; Tenora et al., 1984, 1986) and illustrated above for the type-species of Paranoplocephala. The third pattern, characterised with the formation of 'a uniform, complex reticulum across the entire ventral aspect of the proglottis' (Beveridge, 1994), corresponds with the uterine development of the type-species of Andrya (with the only difference that the reticulum occupies only the median field of the proglottis; see Figure 21). Therefore, Andrya and Paranoplocephala belong to two different groups of genera distinguished from one another by the degree of the uterine reticulation (of. figure 17.89 of Beveridge, 1994). According to Beveridge (1994), the host range of Andrya is restricted to leporid lagomorphs, since Paranoplocephala spp. occur in Holarctic rodents only.
However, the present results exhibit two types of uterine development in the cestodes of the Paranoplocephala-Andrya group from Holarctic rodents. The development of the uterus in the syntypes of P. macrocephala clearly corresponds to that of P. omphalodes. Conversely, the observed early stages of the development of the uterus in P. aquatica and P. ondatrae are reminiscent of the pattern in the typespecies of Andrya. These observations give grounds for the following taxonomic conclusions at the generic level: 1. In agreement with Tenora et al. (1984, 1986) and Beveridge (1994), we recognise Paranoplocephala as a valid genus distinguished from Andrya on the basis of the different uterine development in the type-species of the two genera. 2. The genus Aprostatandrya, with type-species P. macrocephala, is confirmed as a synonym of Paranoplocephala because of the same pattern of uter-
151 ine development in P. omphalodes and P. macrocephala. A similar conclusion was reached by Rausch (1976) and accepted by Tenora et al. (1984, 1986) and Beveridge (1994). However, this suppression of Aprostatandrya has needed to be confirmed from the type-series due to the uncertain status of numerous, variable forms from North American rodents identified as P. macrocephala by previous authors (see Rausch & Schiller, 1949; Rausch, 1976). 3. The genus Paranoplocephala, as defined by Tenora et al. (1986), cannot be regarded as a homogeneous group, since at least P. ondatrae shows an uterine development resembling this in A. rhopalocephala. It should be pointed out, however, that Tenora et al. (1984, 1986) mentioned that some species with inadequately known uterine development had been provisionally placed in Paranoplocephala. If the pattern of the uterine development is the only distinguishing character between the genera Andrya and Paranoplocephala, as suggested by Rausch ( 1976) and Tenora et al. (1984, 1986), then P. aquatica and P. ondatrae should be classified in Andrya. However, the presence of the 'prostatic' cells on the surface of the external seminal vesicle was recently re-evaluated and used at the generic level by Beveridge (1994). He included this character in the generic diagnoses of Andrya and Diandrya and used it in phylogenetic reconstructions. Furthermore, we observed in species with finely reticulated uteri an interesting gradation in 'prostatic' cell development. In A. rhopalocephala, the 'prostatic' cells are large, elongate, intensely stained (the latter suggests contents of secretion); in P. aquatica, these cells are rounded and not intensely stained (without secretory functions?); in P. ondatrae, no 'prostatic' cells are present. This is our first reason for not classifying P. aquatica and P. ondatrae in the genus Andrya. The second reason is the lack of adequate data on early uterine development for most of the species referred to Paranoplocephala by Tenora et al. (1986). A complete revision of this group might show further diversity in the modes of uterine development. Unfortunately, in many species this character needs to be studied on the basis of new, well-relaxed and well-stained specimens, since many of the collected specimens are not in sufficiently good condition to permit an adequate study (e.g.P. sciuri, see above). In summary, the problem for the formulation of reliable generic criteria for the Paranoplocephala-Andrya group is still not solved. We agree with Beveridge (1994) that further detailed study is required to resolve these uncertainties. Since such a study might take an
extended period of time, as a tentative and provisional decision, we propose that the species from lagomorphs be regarded as members of Andrya and those from rodents be referred to Paranoplocephala, in spite of the heterogeneity of the latter genus in terms of uterine development. The criteria used at the species level in Paranoplocephala were reviewed by Tenora et al. (1985, 1986). They regarded as characters of major taxonomic importance: the length of the vagina in relation to the cirrussac; the average diameter of the scolex and the suckers; the number of testes and their distribution; the situation of the ovary (central, poral, aporal); the shape of the seminal receptacle; the position of the genital pores (unilateral, tending to alternation, irregularly alternating); the host range and geographical distribution of the species; and the average diameter of the eggs. They also believed that 'the process of finding further criteria is a completely open matter' (Tenora et al., 1986). On the basis of the observations and comparisons included in this paper, we confirm the taxonomic importance of the above-mentioned criteria at the species level. However, the application of some of them needs more detailed elaboration. The relative length of the vagina to the cirrus-sac was initially used as a species distinguishing character in Paranoplocephala by Tenora & Murai (1980). Later, it was used as a major key character, i.e. 'vagina shorter than 1/2 of the cirrus-sac' or 'vagina longer than 1/2 of the cirrus-sac' (Tenora et al., 1986). For the purposes of further and more detailed comparisons, however, we believe that an adequate measure of this character should be the ratio length of vagina/length of cirrus-sac calculated for each mature proglottis. A more adequate measure is also needed for the asymmetrical disposition of the female genital glands. Such an 'index of asymmetrical situation of female organs' has already been used for the species of the genus Anoplocephaloides Baer, 1923 (see Sato et al., 1993). The present comparisons justify the use of this index for species of Paranoplocephala. Further studies are needed to elucidate the taxonomic importance of the cellular covering of the external seminal vesicle in the genus Paranoplocephala.
Acknowledgements We are grateful to Dr J.R. Lichtenfels (US Department of Agriculture, Beltsville) and Dr E. Murai (Hungarian
152
Natural History Museum, Budapest) for lending specimens and to Dr S.R. Stoitsova (Institute of Microbiology, Sofia) for the critical review of the English text. This investigation was completed with the financial support given by the National Scientific Research Foundation of the Republic of Bulgaria, Grant B44/1991.
References Akhumyan, K.S. (1956) [To the knowledge of the cestode fauna of rodents in Armenia.] Zoologichesla'y Sbornik (Erevan), 9, 171223 [In Russian]. Beveridge, I. (1994) Family Anoplocephalidae Cholodkovsky, 1902. In: Khalil, L.E, Jones, A. & Bray, R.A. (Eds) Keys to the cestode parasites of vertebrates, Wallingford, UK: CAB International, pp. 315-366. Douthitt, H. (1915) Studies on the cestode family Anoplocephalidae. University of lllinois Bulletin, 12, 353-446. Feliu, C., Torres, J., Miguel, J., Casanova, J. C., Ruiz-Olmo, J. & Palazon, J. (1992) Ecological factors conditioning the helminthfauna ofArvicola sapidus (Miller, 1908) (Rodentia: Arvicolidae) in the Iberian Peninsula. In: Schropfer, R. et al. (eds) Semiaquatische S,iugetiere, Wissenschaftliehe Beitr~ige Universit/it. Halle, 98-102. Genov, T. (1964) [On the helminth fauna of muskrat (Ondatra zibethica L.) in Dobrudzha.] Izvesn'ya na Tsentralnata Khelmintologichna Laboratoriya, 9, 97-115 [In Bulgarian]. Genov, T. (1984) [Helminths of insectivorous mammals and rodents in Bulgaria.] Sofia: Publishing House of the Bulgarian Academy of Sciences, 348 pp. [In Bulgarian]. Hunkeler, P. (1972) Les Cestodes parasites des petits mammiferes (Rongenrs et Insectivores) de Cote-d'Ivoire et de Haute-Volta (note preliminaire). Bulletin de la Soci~t~Neuch~teloise des Sciences Naturelles, 95, 121-132. Hunkeler, P. (1974) Les Cestodes parasites des petits mammiferes (Rongeurs et Insectivores) de Cote-d'Ivoire et de Haute-Volta. Revue Suisse de Zoologie, 80, 809-930. Kirshenblat, Ya.D. (1938) [Regularities in the dynamics of the parasiticfauna in murid rodents.] Dissertation. Izdanie Leningradskogo Gosudarstvenogo Universiteta, Leningrad, 92 pp. [In Russian]. Rausch, R.L. (1947) Andrya sciuri n. sp., a cestode from the northern flying squirrel. The Journal of Parasitology, 33, 316-318. Rausch, R.L. (1948) Notes on the cestodes of the genus Andrya Railliet, 1883, with the description ofA. ondatrae n. sp. (Cestoda: Anoplocephalidae). Transactions of the American Microscopical Society, 67, 187-191.
Rausch, R.L. (1976) The genera Paranoplocephala Luehe, 1910 and Anoplocephaloides Baer, 1923 (Cestoda: Anoplocephalidae), with particular reference to species in Rodents. Annales de Parasitologie Humaine et Compar~e, 51, 513-562. Rausch, R.L. (1980) Redescription of Diandrya composita Darrah, 1930 (Cestoda: Anoplocephalidae) from Nearctic marmots (Rodentia: Sciuridae) and the relationships of the genus Diandrya emend. Proceedings of The Helminthological Society of Washington, 47, 157-164. Rausch, R.L. & Schiller, E.L. (1949) A critical study of North American cestodes of the genus Andrya with special reference to A. macrocephala Douthitt, 1915 (Cestoda: Anoplocephalidae). The Journal of Parasitology, 35, 306--314. Ryzhikov, K.M., Gvozdev, E.V., Tokobaev, M.M., Shaldyhin, L.S., Mazaberidze, G.V., Merkusheva, I.V.,Nadtochiy, E.V., Khokhlova, I.G. & Sharpilo, L.D. (1978) [Key to the helminth parasites of rodents from the fauna of USSR. Cestodes and trematodes.] Moscow, Izdatel'stvo 'Nauka', 232 pp. [In Russian]. Sato, H., Kamiya, H., Tenora, F. & Kamiya, M. (1993) Anoplocephaloides dentatoides sp. n. from gray red-backed vole, Clethrionomys rufocanus bedfordiae, in Hokkaido, Japan. Journal of The Helminthological Society of Washington, 60, 105-I 10. Schuster, R. (1987) Beitr~ge zur Parasitenfanna der DDR. 8. Mitteilung: Zur Helminthenfauna von Ondatra zibethica. Angewandte Parasitologie, 28, 21-25. Spasskii, A.A., Romanova, N.E & Naydenova, N.V. (1951) [New data on the parasitic worms of Ondatra zibethica (L.).] Trudy Gel'mintologicheskoy Laboratorff Akademii Nauk SSSR, 5, 4252. Tenora, F. (1956) Prispevek k poznani helmintofauny ondatry pizmove (Ondatra zibethica L.) v CSR. Sbornik Vysoke Skoly Zemedelske a Lesnicke Fakulty v Brne, Rada A, 1, 37-50. Tenora, E & Murai, E. (1978) Anoplocephalidae (Cestoda) parasites of Leporidae and Sciuridae in Europe. Acta Zoologica Academiae Scientiarum Hungaricae, 24, 415-429. Tenom, E & Murai, E. (1980) The genera Anoplocephaloides and Paranoplocephala (Cestoda) parasites of Rodentia in Europe. Acta Zoologiea Academiae Scientiarum Hungaricae, 26, 263284. Tenora, E, Murai, E. & Vaucher, C. (1984) On Anoplocephalidae (Cestoda), parasitizing Rodentia and Lagomorpha in Europe. Parasitologia Hungarica, 17, 51-57. Tenora, E, Murai, E. & Vaucher, C. (1985) On some Paranoplocephala species (Cestoda: Anoploeephalidae) parasitizing rodents (Rodentia) in Europe. Parasitologia Hungarica, 18, 2948. Tenora, F., Murai, E. & Vaucher, C. (1986) OnAndrya Railliet, 1893 andParanoplocephala Luehe, 1910 (Cestoda, Monieziinae). Parasitologia Hungarica, 19, 43-75.
