(Cestoda, Anoplocephalidae), a parasite of sagebrush voles Lemmiscus curtatus (Rodentia) in the USA. František Tenora1, András Gubányi2 & ´Eva Murai2.
Systematic Parasitology 42: 153–158, 1999. © 1999 Kluwer Academic Publishers. Printed in the Netherlands.
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Paranoplocephala maseri n. sp. (Cestoda, Anoplocephalidae), a parasite of sagebrush voles Lemmiscus curtatus (Rodentia) in the USA ´ Murai2 František Tenora1 , Andr´as Gub´anyi2 & Eva 1 Department
of Zoology, Mendel University for Agriculture and Forestry, 61300 Brno, Czech Republic Hungarian Natural History Museum, H–1088 Budapest, Baross u. 13, Hungary
2 Zoological Department,
Accepted for publication 4th April, 1998
Abstract Paranoplocephala maseri n. sp. is described from Lemmiscus curtatus (Cope) in the USA. The new species is related to Paranoplocephala omphalodes (Hermann, 1783), P. caucasica (Kirschenblat, 1938), P. kirbyi Voge 1948, P. microti (Hansen, 1947) and P. macrocephala (Douthitt, 1915) sensu Genov et al. (1996). P. maseri n. sp. differs from P. omphalodes in the position of the genital pores, testes and cirrus-sac; from P. caucasica, in which there is an unarmed cirrus, in both the distribution and larger number of testes; from P. kirbyi in the distribution of the testes, the position of the genital pores and egg dimensions; from P. microti in the distribution and smaller number of testes, the smaller egg dimensions and the position of the genital pores; and from P. macrocephala in the position of genital pores and cirrus-sac.
Introduction We had an opportunity to study cestodes collected by Chris Maser, formerly of the Bureau of Land Management, US Department of the Interior, during the course of surveys of the mammalian fauna of the State of Oregon. The identification of cestodes recovered from sagebrush voles Lemmiscus curtatus (Cope) (syn. Lagurus curtatus) resulted in the description of a new cestode, which we name Paranoplocephala maseri n. sp.
(RLR 39509) – from L. curtatus, female, Jefferson County, Oregon, 17.xi.1969; HNHM 67371 (RLR 39514) – from L. curtatus, male, Klamath County, Oregon, 16.v.1970. Most of the measurements were calculated using an image analysis system on an Olympus BH-2 microscope linked to computer, a grey-scale Panasonic video camera (420 lines) and a high-resolution video digitising card (760 lines). All distance measurements in the paper are given in millimetres unless stated otherwise.
Materials and methods
Paranoplocephala maseri n. sp.
The sagebrush voles Lemmiscus curtatus were collected by C. Maser, who also preserved the helminths. The specimens were stained in acetic carmine and mounted as whole-mounts by Dr R.L. Rausch. The abbreviations for the collections are as follows: HNHM, Parasitological Collection of Hungarian Natural History Museum; CM, Collection of Chris Maser; RLR, Collection of R.L. Rausch. The following cestodes were studied: HNHM 67369 (CM 1998) – from L. curtatus, female, Jefferson County, Oregon, 21.xii.1969; HNHM 67370
Type-material: Holotype: HNHM 67369 – 21.xii.1969, female Lemmiscus curtatus (Cope), Jefferson County, Oregon, complete specimens, deposited in the Parasitological Collection, Department of Zoology, Hungarian Natural History Museum, Budapest. Paratypes: USNPC 87824 (formerly in Hungarian Natural History Museum: HNHM 67370) – 17.xi.1969, female L. curtatus (Cope), Jefferson County, Oregon, deposited in US Department of Agriculture, Biosystematics and National Parasite Collection Unit, Beltsville, Maryland 20705, USA. HNHM 67371 – 16.v.1970,
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154 male L. curtatus (Cope), Klamath County, Oregon, deposited in the Parasitological Collection, Department of Zoology, Hungarian Natural History Museum, Budapest. Etymology: This cestode is named for Chris Maser, Corvallis, Oregon, who collected the specimens. Description Strobila up to 126 long; maximum width, attained in postmature segments, 3.65. Strobila ribbon-like, with serrate margins. All segments wider than long. Length/width ratio of mature segments approximately 1 : 4.79–7.36 (5.89, n = 69), of postmature segments 1 : 5.89–7.58 (6.63, n = 24), of gravid segments: 1 : 3.08–3.84 (3.47, n = 17), with an increase of relative length posteriorly. Scolex and neck well developed and separated from each other. Scolex 0.54– 0.67 × 0.87–1.16. Suckers of holotype 0.44–0.47 (0.46, n = 3) in diameter (Figure 1). Genital organs visible before external segmentation becomes evident. Genital pores unilateral. Genital opening near middle of segment margin (Figure 2). Excretory system simple, with paired dorsal and ventral canals. Ventral canals c. 0.07 in diameter, connected at posterior margin of segment by wide transverse canal. Cirrus-sac 0.14 long by 0.06–0.08 wide in mature segments, 0.11–0.14 long by 0.04–0.05 wide in gravid segments (Figure 2). In mature segments, cirrus-sac never reaches ventral longitudinal excretory canals (Figure 3); in gravid segments it occasionally reaches ventral excretory canals, but never overlaps. Cirrus very small, covered by small fine spines in ductus cirri (Figure 2). Large internal seminal vesicle present. External seminal vesicle tubular, coiled, lightly stained (Figure 2). Testes spherical, 0.03–0.05 (mean 0.04, n = 20) × 0.03–0.04 (mean 0.03), 40–50 in number, distributed in aporal half of segment; occasionally isolated testes present anterior to ovary (Figure 3). Vagina enlarged, opens posteriorly to cirrus-sac (Figure 2). Ovary 0.34–0.46 in width, situated ventrally, almost in poral part of the segment (Figure 3), lobed in first mature segments, compact in last mature segments. Vitelline gland poral, 0.18–0.24 in width. Uterine duct passes antero-ventrally, forming irregularly transverse tube, extending across ventral excretory canals (Figure 4), but, in postmature segments, beyond ventral longitudinal excretory canals; uterus increases in width, gradually becoming fenestrated or reticulate (Figure 5). At same time, uterus gradually fills space between ventral longitudinal ex-
cretory canals with slightly irregular margins and internal reticulation (Figure 5). In first gravid segments, part of uterus crosses poral and aporal ventral excretory canals, fully reticulate (Figure 6). Uterus between poral and aporal canals develops anterior and posterior diverticula (Figure 6). In gravid segments uterus sacciform without diverticula. Egg thin-walled, spherical, 37–42.5 µm in diameter (mean 40.1 µm, n = 20). Pyriform apparatus well developed.
Discussion P. maseri n. sp. is a typical representative of Paranoplocephala Lühe, 1910. Baer (1927), Joyeux & Baer (1936), Spasskii (1951), Rausch (1952), LópezNeyra (1954), Erhardová & Rysavy (1955), Yamaguti (1959), Tenora (1976) and Ryzhikov et al. (1978) characterised the genus Paranoplocephala as having a simple, tubular uterus. Rausch (1976), however, showed that in the type-species the uterus was in fact reticulate and removed those species with simple tubular uteri to the genus Anoplocephaloides Baer, 1923. Rausch’s (1976) conclusion was accepted by Tenora & Murai (1980), Tenora et al. (1981–1982, 1984, 1985, 1986b), Schmidt (1986) and Beveridge (1994). In order to solve the problem, the development of the uterus of Paranoplocephala must be taken into account. The developmental stages of a “paranoplocephaloid” uterus are as follows: 1. Uterus antero-ventral, transverse, at first rod-like, later tubular or band-like, sometimes irregular. 2. Uterus in postmature segments extends beyond ventral excretory canals, fenestrated or reticulate. Inner region of uterus between ventral excretory canals sometimes fenestrated or reticulate; margins more or less irregular in form. 3. In the pre-gravid segments, lateral part of uterus beyond ventral longitudinal excretory canals fully fenestrated or reticulate. Uterus between ventral longitudinal excretory canals forms a transverse stem with anterior and posterior diverticula, which are fenestrated or reticulate. 4. In gravid segments, inner structure of uterus is saccate; eggs with well-developed pyriform apparatus. Paranoplocephala maseri n. sp. is related to P. omphalodes (Hermann, 1783), P. caucasica (Kirschenblat, 1938), P. kirbyi Voge, 1948, P. microti (Hansen, 1947), and P. macrocephala (Douthitt, 1915) sensu Genov et al. (1996). All these species are characterised
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Table I. Comparison of some characteristics of Paranoplocephala omphalodes, P. microti, P. kirbyi, P. caucasica, P. macrocephala and P. maseri n. sp. P. omphalodes Tenora & Murai, 1980 Europe Microtus arvalis
P. omphalodes Rausch, 1976 USA Microtus oeconomus, M. miurus, M. abbreviatus
P. microti Hansen, 1947 USA Microtus onchogaster
P. kirbyi Voge, 1948 USA Microtus californicus
P. caucasica Kirschenblat, 1938 Georgia Microtus socialis
P. macrocephala Genov et al., 1996 USA Geomys bursarius
P. maseri n. sp. Present data USA Lemmiscus curtatus
Length of strobila Maximum width Scolex width Suckers Genital pores
128 3 0.88 0.36–0.40 Irregularly alternating
162–198 4–6 0.80–1.02 − Irregularly alternating
0.21–0.30 × 0.08–0.12 – + +
160–270 2.689–2.839 0.880–1.029 0.332–0.398 Irregularly or in alternating series 0.144–0.199 ?
100–170 0.9–1.3 0.40–0.79 0.26–0.33 Unilateral or alternating 0.130–0.170 −
90 2 0.711–0.722 0.358–0.402 Alternating in large series 0.152–170 × 0.054–0.63 +
Up to 126 3.7 0.87–1.16 0.44–0.47 Unilateral
Cirrus-sac Cirrus-sac reaching excretory canals (+, −) Cirrus Distribution of testes
90–200 1.7–2.09 0.85–1.26 0.31–0.49 Irregularly or in alternating series 0.178–0.233 − Spinose Overlapping aporal ventral longit excr. canal
– Overlapping aporal ventral longit. excr. canal
Aspinose Overlapping aporal ventral longit. excr. canal
Spinose Extending to poral lateral field, overlapping lobes of ovary
Spinose Not extending over apor. long ventral ex. canal
25–35 0.032–0.033
24–35 0.030–0.034
26–34 0.028–0.038
42–57 −
41–50 0.037–0.042
No. of testes Diameter of egg
Spinose Aporal margin of ovary, extending to aporal ventral longit excr. canal 45 0.034
Spinose Aporal margin of ovary to aporal ventral longit excr. canal occasionaly extending passed it − 0.036–0.044
0.11–0.14 −
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Author Distribution Host(s)
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Figures 1–2. Paranoplocephala maseri n. sp. 1. Schematic drawings of scolex. 2. Genital opening, cirrus-sac, and vesicula seminalis interna and externa. Scale-bars: 1, 0.25 mm; 2, 0.15 mm.
by the location of testes, mostly in the aporal half of mature segments. Their hosts are arvicolid rodents, except for P. macrocephala, and all are described from the Nearctic region, except for P. caucasica. A comparison of some morphometric characteristics of these species and P. maseri n. sp. is given in Table I. P. omphalodes is reported from the Holarctic region and parasitises the genus Microtus (see Rausch, 1976, 1982, 1994; Haukisalmi et al., 1995). P. maseri n. sp. differs from P. omphalodes in the following characters: genital openings unilateral, the cirrus-sac does not overlap the poral ventral excretory canal and the testes do not overlap the aporal ventral excretory canal. P. caucasica is known from the Palaearctic region (Spasskii, 1951; Ryzhikov et al., 1978). It was described originally as a member of the genus Andrya Railliet, 1893, and later transferred by Spasskii (1951) to Aprostatandrya Kirschenblat, 1938 and by Tenora et al. (1984) to Paranoplocephala Lühe, 1910. Rausch & Tiner (1949) found a striking morphological similarity between P. caucasica and P. microti. P. maseri n. sp. differs from P. caucasica in its armed cirrus and the position and larger number of testes. It can also be distinguished from P. caucasica by the size of the eggs. Host-specificity and the geographical distribution also support the difference found between the two species. P. kirbyi is known only from the Nearctic region (see Voge, 1948; Smith, 1986). Rausch (1952a, 1957) considered P. kirbyi conspecific with Andrya macrocephala Douthitt, 1915.P. maseri n. sp. can be
distinguished from P. kirbyi by its greater egg size, the location of the testes, the position of the genital pores and host-specificity. The cirrus cannot be compared because its morphology in the latter species is unknown (Voge, 1948). P. microti, originally described in the USA, parasitises rodents in the Palaearctic region (Erhardova, 1956; Egorova & Nadtochi, 1975; Ryzhikov et al., 1975; Tenora et al., 1986a). However, in the absence of a direct comparison of specimens from the two continents, the Holarctic distribution of P. microti is uncertain (Rausch, 1994). This species has been discussed by Rausch (1948), Rausch & Tiner (1949) and Tenora et al. (1986a); however, it was omitted from consideration by Schmidt (1986). P. maseri n. sp. differs from P. microti in the following characters: smaller number and different location of the testes, and smaller egg sizes. P. microti parasitises Microtus spp., whereas P. maseri has been recovered only from Lemmiscus curtatus. P. maseri n. sp. is also related to P. macrocephala (sensu Genov et al., 1996), a parasite of Geomys bursarius. It differs from this species in the different form of the uterus and different positions of the genital openings and cirrus-sac (see Genov et al., 1996; Figures 4–6 in the present paper). Acknowledgements The cestodes were made available for study by Prof. R.L. Rausch, Department of Comparative Medicine, University of Washington, for which we are grateful.
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Figures 3–6. Paranoplocephala maseri n. sp. 3. Mature segment. 4. Uterus in post-mature segment. 5. Uterus in pre-gravid segment. 6. Uterus in gravid segment. Scale-bars: 3, 0.41 mm; 4, 0.53 mm; 5–6, 0.25 mm.
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158 Special thanks are due to two anonymous reviewers who provided helpful comments on a draft of this manuscript.
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