Parasit. Hung. 13. 1980.

The System of Cestodes of the Suborder Catenotaeniata Spassky, 1963

Dr. Frantisek TENORA — Dr. Santiago MAS-COMA— Dr. Éva MURAI — Dr. Carlos FELIU

Zoological Department of the University of Agriculture, Brno, Czechoslovakia — Department of Parasitology, Faculty of Pharmacy, University of Barcelona, Barcelona, Spain — Zoological Department of the Hungarian Natural History Museum, Budapest, Hungary

"The system of cestodes of the suborder Catenotaeniata Spassky, 1963" - Tenora, F. - Mas-Coma, S. - Murai, É. - Feliu, C. - Parasit. Hung. 13_. 39-57. 1980.

ABSTRACT. A new systematic division of cestodes of the suborder Catenotaeniata Spassky, 19 63 is presented. The single family Catenotaeniidae Spassky, 1950 belong­ ing to this suborder is divided into two subfamilies: Catenotaeniinae Spassky, 1949 and Skrjabinotaeniinae Genov et Tenora, 1979. The subfamily Catenotaeniinae in­ cludes the genera Catenotaenia Janicki, 1904, Hemicatenotaenia (Tenora, 1977) Genov et Tenora, 1979, Pseudocatenotaenia gen.nov. and Quentinotaenia gen.nov. The subfamily Skrjabinotaeniinae comprises the Skrjabinotaenia Akhumyan, 1946 and Meggitina Lynsdale, 1953. A hypothesis on the evolution of cestodes of the suborder Catenotaeniata is discussed.

INTRODUCTION

The suborder Catenotaeniata was established by SPASSKY (19 63) for the cestodes of the family Catenotaeniidae Spassky, 1950. The separation of this family from the suborder Anoplocephalata was necessary with respect tó its morphological-anatomical characters, dif­ ferent process of evolution, specialization (during the life-cycle) to invertebrates and to a single order of - . Characteristic features of the larvae of these cestodes are the presence of the apical sucker. In adult specimens, the topography of body organs is arranged in a quite special manner: originally strong asymmetrically formed ovary (except Quentinotaenia) and originally markedly elongated uterus (except in Meggittina). FREEMAN (19 73) pointed out independent evolutionary branches of cestodes of the families Catenotaenii­ dae, Proteocephalidàe and Taeniidae (which according to SPASSKY, 1978 are taxa at the level of suborders: Catenotaeniata, Proteocephalata and Taeniata) and documented a principal dif­ ference between the evolution of these cestodes and of those of the family Anoplocephalidae (Anoplocephalata). Thus, the scheme of FREEMAN (1973) is near to the classification of LOPEZ-NEYRA (1947) who included already the genus Catenotaenia in the family Taeniidae. In spite of the above facts the system proposed by SPASSKY in 1963 has not been generally accepted in the helminthological literature. Often the family Catenotaeniidae has not even been recognized and the of this family have been ascribed to the subfamily Catenotaeniinae or Anoplocephalinae (fam.: Anoplocephalidae) belonging to the suborder Ano­ plocephalata (see GENOV and TENORA, 1979). Our studies of the material (see below) and literature revealed that with regard to the present state in the cestode , Catenotaeniidae can be placed as a single known family to the suborder Catenotaeniata. On the other hand, the studies of the peculiarities of these cestodes, not only from morphological, but also ecological and paleobiological view­ points, let us to the conclusion that the present system of Catenotaeniata should be revised.

MATERIAL

The material mentioned by GENOV and TENORA (1979) and original material from Spain and Hungary were used for the present studies: a) The material from Spain:

1. - Catenotaenia pusilla (Goeze, 1782). Hosts: Mus musculus Linnaeus, 1758 and Mus spretus Lataste, 1883. - Localities: La Floresta (prov. Barcelona), Amposta (prov. Tarragona) and Villanueva de Sijena (prov. Huesca). 2. - Pseudocatenotaenia matovi (Genov, 1971). Host: Apodemus sylvaticus Lin­ naeus, 1758. - Localities: Figueras and Estartit (prov. Gerona) and La Guingueta (prov. Lérida). 3. - Skrjabinotaenia lobata (Baer, 1925). Host: Apodemus sylvaticus Linnaeus, 1758. - Localities: All N.E. of Spain (prov. Barcelona, Tarragona, Gerona, Lérida and Huesca).

b) The material from Hungary:

4. - Catenotaenia pusilla (Goeze, 1782). Host: Mus musculus spicilegus Petényi, 1844. - Localities: Orgovány (Com. Bács-Kiskun), Nagyiván (Com. Hajdú-Bihar), Tákos (Com. Szabolcs-Szatmár), Budapest-Óbuda, Kosd, Nagykovácsi (Com. Pest), Bakonynána, Nagyvázsony (Com. Veszprém). 5. - Skrjabinotaenia lobata (Baer, 192 5). Host: Apodemus flavicollis Melchior, 1834.- Localities: Aranyosgadány (Com. Baranya), Brennbergbánya, Sopron (Com. Győr-Sopron), Hajdúbagos, Űjszentmargita (Com. Hajdú-Bihar), Kisnána (Com. Heves), Budakeszi, Ber- necebaráti-Deszkáspuszta (Com. Pest), Somogyszob Lake Baláta (Com. Somogy), Balaton- csicsó, Nagyvázsony, Tihany, (Com. Veszprém), Vállus (Com. Zala). - Host: Apodemus agrárius Pallas, 1771. - Locality: líjszentmargita (Com. Hajdú-Bihar); - Host: Apodemus sylvaticus Linnaeus, 1758. - Localities: Tákos-Bockerek (Com. Szabolcs-Szatmár), Tihany. (Com. Veszprém), Zajk (Com. Zala). - Host: Microtus agrestis Linnaeus, 1761. - Locality: Oriszentpéter (Com. Vas).

RESULTS

Suborder CATENOTAENIATA'Spassky, 1963

Description (after SPASSKY, 1963): Cyclophyllidea of flat bodies. Strobila craspe- dote or acraspedote. Larval stages of merocercoid type provided with apical sucker and de­ veloping in invertebrates. Larvogenesis without metameria stage. Basic stem of uterus ly­ ing longitudinaUy, giving off side branches. Testes situated behind female genital organs, on their sides or in front of them. Adult specimens parasitise in rodents. Type family: Catenotaeniidae Spassky, 1950.

Family CATENOTAENIIDAE Spassky, 19 50

Description (after GENOV and TENORA, 1979): Catenotaeniata of small to medium size. Scolex rounded or semioval, and provided with four suckers. Rostellum and rostellar hooks lacking. Mature segments are elongated either transversely or longitudinally, similar to gravid segments. Genital apparatus is unpaired. Testes situated either in the lower part of proglottids and do not surround the ovary, or surround the cvary in various ways accord­ ing to its situation. Vitelline gland lies near the poral part of proglottids or posteriorly to ovary. Ovary is asymmetrical (except Quentinotaenia), its anterior margin either overlaping genital openings or reaching to the level of these openings. Openings of genital organs situat­ ed either in the lower part of anterior third of proglottids near the upper margin of the an­ terior third of proglottids, or near the anterior part of proglottids. Vas deferens is tubular or ribbonlike; the cirrus sac. contains a cirrus with or without spines. Vesicula seminalis externa and interna absent. Vagina situated posteriorly to the openings of male genital or­ gans. Uterus consisting of a central stem giving off side branches, lateral branches bearing secondary branches. The excretory system comprises longitudinal and transverse stems or a large number of longitudinal stems with processes. Larval stage of meroceroid type devel­ oping in arthropods. It is provided with an apical sucker which may remain even in mature specimens. Eggs are oval and their surface is smooth or with processes. Oncosphere pos- sesse« an oval membrane or a membrane with processes. Adult specimens parasitise rodents. Type genus: Catenotaenia Janicki, 1904. Figs. 1-13: Schematic illustration of principal morphological characters of cestodes of the genus Meggittina Lynsdale, 1953 (Figs 1-4) and Skrjabinotaenia Akhumyan, 1946 (Figs. 5-13) 1 = Meggittina aegyptica (Wolfgang, 1956); 2 = M. gerbilli (Wertheim, 1954); 3 - M. criceto- mydis (Hockley, 1961); 4 = M. baeri Lynsdale, 1953; 5 = Skrjabinotaenia lobata (Baer, 1925)- fully gravid segments; 6 = S, occidentalis Hunkeler, 1972 - fully gravid segment; 7 - S, ora- nensis (Joyeux et Foley, 1930); 8 = S. compacta (Ortlepp, 1962); 9 = S. madagascariensis Quentin et Durette-Desset, 1974; 10 = S. pauciproglottis Quentin, 1965; 11 = S. media Quen­ tin, 1971; 12 = S. lucida (Ortlepp, 1962) - fully gravid segments; 13 = S. psammomi Mikhail et Fahmy, 1969 - fully gravid segment 1. Subfamily CATENOTAENIINAE Spassky, 1949

Description (after GENOV and TENORA, 1979): Cestodes of the family Catenotaenii­ dae. Testes situated only in lower part of proglottids, not surrounding ovary from lateral and dorsal side. Testes situated between lateral excretory canals or overlapping them; they may be divided partly or completely into two groups. Genital openings situated in lower part of an­ terior third of proglottids. Type genus: Catenotaenia Janicki, 1904.

2. Subfamily SKRJABINOTAENIINAE Genov et Tenora, 1979

Description (after GENOV and TENORA, 1979): Cestodes of the family Catenotaenii­ dae. Scolèx semioval or rounded. Testes never restricted to the lower part of proglottids, but surrounding ovary in various ways, and do not overlap lateral excretory canals. They may be divided into two groups. Genital openings in anterior part of upper third of proglot­ tids, mostly in the same level like the anterior margin of the ovary. Ovary asymmetrical, its larger part mostly situated in aporal part of proglottids. Type genus: Skrjabinotaenia Akhumyan, 1946. Note: WERTHEIM (1954) described a new genus Rajotaenia. SPASSKY (1955) clas­ sified the genus Rajotaenia Wertheim, 1954 as a synonym of the genus Skrjabinotaenia Akhu- myan, 1946 which belongs to the family Catenotaeniidae Spassky, 19 50. YAMAGUTI (1959) placed the genus Rajotaenia into the family Anoplocephalidae Cholodkowsky, 1902. He con­ sidered the genus Rajotaenia monotypic within the subfamily Rajotaeniinae Yamaguti, 1959. JOYEUX and BAER (1961) discussed Skrjabinotaenia Akhumyan, 1946, Meggittina Linsdale, 1953 and Rajotaenia Wertheim, 1954 as synonyms of the genus Catenotaenia Janicki, 1904. TENORA (1964) held the genus Rajotaenia Wertheim, 1954 and the genus Meggittina Linsdale, 19 53 as synonyms of the genus Skrjabinotaenia and the subfamily Rajotaeniinae as synonym of the family Catenotaeniidae. On the other hand SPASSKY (19 78) contrary from 1955 accept­ ed Rajotaenia Wertheim, 1954 as a valid genus. GENOV and TENORA (1979) defined a new subfamily - Skrjabinotaeniinae - within the family Catenotaeniidae; this taxon includes only Skrjabinotaenia Akhumyan, 1946 with synonyms Rajotaenia Wertheim, 1954 and Meggittina Lynsdale, 1953. Thispaper demonstrates (see the following text) that the genus Rajotaenia Wertheim, 1954 is a synonym of the genus Meggittina Lynsdale, 1953 and not of Skrjabinotaenia Akhu- myan, 1946. Only the absence of cirrus sac in Rajotaenia (compare in WERTHEIM, 19 54, YAMAGUTI, 1959) indicates that Rajotaenia Wertheim, 1954 is a valid taxon. JOYEUX and BAER (1961) contrary to WERTHEIM (1954) drew Rajotaenia gerbilli Wertheim, 1954 with a cirrus sac. It results from the data mentioned above that the genus Rajotaenia Wertheim, 1954 cannot be the type genus for the subfamily Rajotaeniinae Yamaguti, 1 959 not only due to the fact that it is a synonym of the genus Meggittina Lynsdale, 19 53 but also because the sub­ family Rajotaeniinae Yamaguti, 1959 had been transferred from the family Anoplocephalidae into the family Catenotaeniidae and synonymized with it as early as in 19 64. On the other hand the existence of the taxon Skrjabinotaeniinae Genov et Tenora, 19 79 is fully substantiat­ ed because Skrjabinotaenia (classified as early as in 1946) represents its type genus.

SYSTEMATIC S AND TAXONOMY OF THE SUBFAMILY CATENOTAENIINAE

1. Genus Catenotaenia Janicki, 1904

Description: Cestodes of the family Catenotaeniidae, subfamily Catenotaeniinae. Proglottids craspedonte. Scolex rounded or semioval, neck present. Gravid proglottids al­ ways longer than wide. Overy strongly asymmetrical. Anterior margin of ovary always ex­ ceeding the level of genital openings. Testes situated posteriorly to female organs, do not across the longitudinal excretory canals. Eggs oval, oncosphere provided with oval mem­ brane, without processes. Larval stage of merocercoid type developing in arthropods and provided with apical sucker which may prevail even in mature specimens. Adult specimens are parasitic in rodents. Distribution: Holarctic and Ethiopian Region. Figs. 14-19: Principal morphological-anatomical characters of type species of the genera of the suborder Catenotaeniata Spassky, 1963 14 = Hemicatenotaenia (Tenora, 1977) Genov et Tenora, 1978: H. geosciuri (Ortlepp, 1938) after Ortlepp, 1938; 15 = Skrjabinotaenia Akhumyan, 1946: S. oranensis (Joyeux et Foley, 1930), after Quentin, 1971; 16 = Quentinotaenia gen. nov. : Q. mesovitellinica (Arandas Régo, 1967; 17 = Pseudocatenotaenia gen. nov.: P. matovi (Genov, 1971), after Genov, 1971; IS = Catenotaenia Janicki, 1904: C. pusilla (Goeze, 1782), after Mészáros and Murai, 1979; 19 = Meggittina Lynsdale, 1953: M. baeri Lynsdale, 19 53, after Lynsdale, 1953. Type species: Catenotaenia pusilla (Goeze, 1782) (Fig. 18) Deposition of holotype of type species: not mentioned in the literature. The genus Catenotaenia Janicki, 1904 further includes the following species: C. den- dritica (Goeze, 1782), C. rhombomydis Schultz et Landa, 1934, C. linsdalei Mcintosh, 1941, C. ris Yamaguti, 1942, C. cricetorum Kirschenblat, 1949, C. reggiae Rausch, 1951, C. pe- romysci Smith, 1954, C. laguri Smith, 1954, C. kirgizica Tokobaev, 1959, C. asiatica Te- nora et Murai, 1975, C. kullmanni Tenora, 1977, C. afghana Tenora, 1977.

2. Genus Hemicatenotaenia (Tenora, 1977) Genov et Tenora, 1979

Syn. : Catenotaenia (Hemicatenotaenia) Tenora, 19 77 Description: (after GENOV et TENORA, 1979): Cestodes of the family Catenotaenii­ dae, subfamily Catenotaeniinae. Neck present. Proglottids craspedote. Ovary asymmetrical, its anterior margin not exceeding the level of genital openings. Testes situated posteriorly to female organs, do not across the longitudinal excretory canals. Life-cycle unknown. Eggs possessing oncosphere provided with membrane, with or without protrusions. Adult speci­ mens are parasites of rodents Xerini in Africa. Type species: Hemicatenotaenia geosciuri (Ortlepp, 1938) n. comb. (Fig. 14) Syn. : Catenotaenia geosciuri Ortlepp, 1938; Catenotaenia (Hemicatenotaenia) geo- sciuri Ortlepp, 1938 sensu Tenora, 1977. Deposition of holotype of type species: Onderstepoort Helminthological Collection, South Africa. The genus Hemicatenotaenia further includes: H. chabaudi (Dollfus, 1953). It is worth consideration whether the cestodes found by JOYEUX et BAER, 1945 in Xerus rutilus and Euxerus erythropus in Africa and named Catenotaenia geosciuri do not belong to an in­ dependent species of the genus Hemicatenotaenia. According to these authors, their material differs from H. geosciuri in these characters: number of uterine branches - 33-40 x2 (H.g. ): 12-18 x 2, different position of testes - divided into two groups (H. g. ): they form a single group. In the last characters the material of JOYEUX et BAER, 1945 is most closely related to H. chabaudi.

3. Genus Pseudocatenotaenia gen.nov.

Description: Cestodes of the family Catenotaeniidae, subfamily Catenotaeniinae. Mature segments quadrate or wider than long, gravid segments longer than wide. Scolex semioval, neck present. Strobila acraspedonte. Ovary situated in upper half of segments, asymmetrical, its upper part overlapping opening of genital organs. Branches of ovary reach­ ing lateral excretory canals or overlapping them. Vitelline gland in poral part of segments posterior to uterus, in mature segments overlapping lateral excretory canals. Testes situat­ ed in lower half of segments, overlapping lateral excretory canals in both poral and aporal part. Cirrus sac relatively short, not reaching dorsal to excretory canal. Uterus with lateral branches overlapping excretory canals bilaterally. Eggs oval, with a process on surface, bi­ lateral. Oncosphere provided with membrane, without processes. Life-cycle unknown. Adult specimens parasitic in rodents, particularly Muridae of the genus Apodemus in the Palae- arctic Region. Geographical distribution: reported from the USSR (Crimea Region), Bulgaria and Spain. Type species: Pseudocatenotaenia matovi (Genov, 1971) n. comb. Syn. : Catenotaenia matovi Genov, 1971. Deposition of holotype of type species: Central Laboratory of Helminthology, Bul­ garian Academy of Sciences, Sofia, Bulgaria.

Figs. 20-25: Pseudocatenotaenia matovi of Apodemus sylvaticus from Spain 20 = Scolex of young specimen showing the rest of the larval apical sucker; 21 = scolex of adult specimen; 22 ? sexual mature segment; 23 = gravid segment; 24 = eggs

Differential diagnosis: Cestodes of the genus Pseudocatenotaenia gen. nov. differ from the known genera of the subfamily Catenotaeniinae in the following principal characters: The testes overlap dorsal excretory canal bilaterally. Cirrus sac is very short, neither over­ lapping and nor even reaching dorsal excretory canal. Ovary and uterine branches tend to overlap dorsal excretory canals. The cestodes of the genus Pseudocatenotaenia are very similar and related in their morphology to those of the genus Skrjabinotaenia, particularly S. lobata: scolex semioval, neck present, strobila acraspedote. Last but not least the zoogeographical distribution should be pointed out. This is an Eumediterranean element, hitherto reported only from rodents of the genus Apodemus.

Pseudocatenotaenia matovi (Genov, 1971) n. comb. (Figs. 17 and 20-25)

Host: Apodemus sylvaticus; Linnaeus, 1758. - Extensity of the invasion: A, sylva­ ticus - in 4 of 688 specimens investigated (0.005%). - Localities: Figueras and Estartit (prov. Gerona) and La GMngueta (prov. Lérida) Catalonia: Spain. Description (based on 9 specimens, all dimensions in mm): Cestodes with a total length ranging from 35 (younger specimens) to 100 (adults). Width varies considerably along the strobila, from 1. 5 - 1.8 (average 1.6) at the mature segments, to 1.8 - 2.-2 (2.0) at the last gravid ones.

Table 1

The dimensions of Pseudocatenotaenia matovi (Genov, 1971) (all dimensions given in mm)

Body length 14. 77 - 45. 15 24 - 26 35 - 100 Body width 1. 835 - 2. 321 1.8408 - 2.7720 1.5- 2. 2 Scolex diameter 0. 313 - 0. 422 0. 3032 - 0. 4764 0. 250 - 0. 417 Suckers' diameter 0. 126 - 0. 149 0. 1222 - 0. 1357 0. 75 - 0. 154 Neck length 0. 738 - 1. 688 0. 3248 1.0 - 1. 5 Number of segments of strobila 40 - 50 73 - 77 50 - 70 Number of testes 140 - 160 140 150 - 180 Testes' diameter 0. 062 - 0. 083 0. 0226 - 0.0633 0. 050 - 0. 086 Cirrus sac length 0. 083 - 0. 06+ 0.228 - 0.230++ 0. 1991 0. 164 - 0. 282 Vagina length 0. 358 - 0. 379 0.4433 0. 342 - 0. 522 Primary branches of uterus 7-9x2* 14 - 18 x 2 12 - 15 x 2 12 x 2** Hosts A. flavicollis A. flavic ollis A. sylvaticus A. sylvaticus Distribution Bulgaria USSR Spain Author Genov, 1971 Zavaleeva, 1974 Present material

+ uncorrect dimension in the description Genov (1971) ++ correct dimension in holotypus 3t in description Genov (1971 ** in fig. 10 - Genov (1971)

The scolex, the diameter of which ranges from 0.250-0. 417 (0.374), has circular suckers with a diameter from 0. 075-0. 154 (0. 122). The rudiments of an apical sucker are

Fig. 25: Egg of Pseudocatenotaenia matovi (Photo: S. Mas-Coma) Fig. 26: Eggs of Skrjabinotaenia lobata (Photo: É. Murai) still visible in young specimens (Fig. 20). Under that structure, if present, there is the be­ ginning of the excretory ducts (a ventral and a dorsal pair) running down at a distance of a- bout 0. 060 from the scolex external wall and 0.282-0.400 (0.331) from the sexual segments external wall. The diameter of the ventral ducts ranges between 0.038-0.060 (0.045) at the level of the sexual segments. The strobila is made up of 50-70 segments of the craspedote type, with a relative in­ crease length posteriorly. The first proglottids are wider than long; sexual mature ones are almost square, of 1.2-1.6/1. 5-1. 8 (1.5/1.6) of length/width (ratio of length and width 1:1. 1); gravid segments of 2.7-3.4/1.8-2.2 (2.9/2.0) of length/width (ratio of length and width 1. 5:1). The neck is rather short, between 1.0-1. 5 (1.4), variability depending on fixation. The genital pores open at the end of the first third of the proglottids, alternating ir­ regularly (in 50 segments studied, it was 30 times on the right, 20 times on the left; the high­ est number of consecutive segments with the pore on the same side being 6). The number of the testes ranges from 150-180 (170), the diameter of which being 0.050-0.086 (0.066). About 50 or 60 of them overlap excretory ducts bilaterally (Fig. 22). The cirrus sac measures 0. 164-0. 282/0. 077-0. 096 (0. 229-0. 087) and never reaches the lat­ eral excretory duct. The cirrus is unarmed, ranging from 0. 134-0.268 (0.201). Vas deferens showing prostatic cells clearly visible at its end. The ovary is markedly lobed, occuppying the anterior half part of the sexual pro­ glottid and overlapping excretory ducts bilaterally. The vitelline gland has a diameter ranging from 0. 522-0.671 (0.564); it is always displaced porally and placed behind the ovary, being less lobed than the ovary and overlapping excretory ducts porally. The vagina runs nearly parallel to the male deferent duct, measures 0.345-0. 522 (0. 462) and ends up at an almost completely spherical seminal receptacle of 0.089-0. 134 (0. 108) of diameter. Uterus begins to develop in the 20th or 24th sexual segment. The number of uterine main lateral branches is from 12-15 x 2 (13x2) at the gravid segments (Fig. 23). Lateral branches of uterus always across excretory ducts bilaterally. Eggs rectangular, presenting double external membrane expanding in two lateral alar processes, measuring 0.028-0.033/ 0.11-0.15 (0.030/0.013) (Fig. 24). The oncosphere is of 0. 018-0. 022/0. 007-0. 011 (0,020/ 0. 008). The size of the embryonal hooks is about 0. 004-0. 005 (0. 004). Note: The material found in Spain is in principle identical with C. matovi described by GENOV (1971). It differs particularly in the length of cirrus sac, number of uterine branches and situation of uterine branches in relation to excretory organs. Our study of the material of GENOV (19 71), as well as our correspondence with him, revealed that these data are incorrect in the original description of C. matovi. The species C. matovi was also re­ ported by ZAVALEEVA (1974) from the Crimea Region (USSR). The metrical data are com­ pared in Table 1. The table shows that the material from the USSR, Spain and Bulgaria is not identical in all characters. Since the criteria for species differentitation in the genus Pseudo­ catenotaenia are not exactly defined, we leave the material from the USSR, Bulgaria and Spain under the name Pseudocatenotaenia matovi (Genov, 1971) for the time being. It is quite likely that more species are involved.

4. Genus Quentinotaenia gen.nov.

Description: Cestodes of the family Catenotaeniidae, subfamily Catenotaeniinae. Mature and gravid segments longer than wide. Genital pores in anterior fourth of segments, regularly alternating. Scolex with four large suckers. Neck absent. Ovary in upper half of segments, almost symmetrical, horseshoe-shaped, its larger portion situated under openings of genital organs. Upper portion of ovary overlapping the level of genital openings. Seminal receptacle situated inside horseshoe-shaped ovary. Vitelline gland compact, situated pos­ teriorly to ovary, upper margin reaching lower branches of ovary. Testes lying posteriorly to vitelline gland, between lateral excretory canals. Exact morphology of eggs unknown. Life- cycle unknown. Adult specimens parasitic in Caviomorph of the family Caviidae in the Neo­ tropical Region. Type species: Quentinotaenia mesovitellinica (Arandas Régo, 1967) n. comb. (Fig. 16) Syn. : Catenotaenia mesovitellinica Arandas Régo, 19 67. Deposition of holotype of type species: Institute Oswaldo Cruz, Rio de Janeiro, South America. This genus is monotypic. Differential diagnosis: The cestodes of the genus Quentinotaenia differ from other hitherto known genera of the subfamily Catenotaeniinae particularly in the following features: Ovary is not strongly asymmetrical, but almost symmetrical and horseshoe-shaped. Vitelline gland does not enter the ovary from the poral side, but is situated posteriorly to ovary. The seminal receptacle lies between the ovary and vitelline gland. A characteristic feature of cestodes of the genus Quentinotaenia is also their zoogeographical distribution: they are the only members of the suborder Catenotaeniata occurring in the Neotropical Region.

SYSTEMATICS AND TAXONOMV OF THE SUBFAMILY SKRJABINOTAENIINAE

1. Genus Skrjabinotaenia Akhumyan, 1946 emend.

Syn. : Catenotaenia (Spasskiela) Tenora, 19 59. Description: Cestodes of the family Catenotaeniidae, subfamily Skrjabinotaeniinae. Scolex with 4 spherical suckers. Neck present or absent. Genital apparatus unpaired. Testes numerous, surrounding ovary in various ways: a) from lateral and ventral side, b) from lat­ eral side, c) sometimes circumovarial. Testes may be divided into two groups. Strobila acraspedote or craspedote. Full gravid proglottids longer than wide. Basic longitudinal stem with numerous side branches, shorter than the stem. Eggs possessing oncosphere provided with membrane with or without protrusions. Life-cycle unknown. Adult specimens parasitic in rodents. Distribution: Palaearctic and Ethiopian Region. Type species: Skrjabinotaenia oranensis (Joyeux et Foley, 1930) Akhumyan, 1946 (Fig. 15). Syn. : Catenotaenia oranensis Joyeux et Foley, 1930. Deposition of holotype of type species: Laboratoire de Zoologie, Université de Neu- châtel, Suisse. The genus Skrjabinotaenia further includes the following described species: S. lobata (Baer, 1925), S. capensis (Ortlepp, 1940), S. lucida (Ortlepp, 1962), S. compacta (Ortlepp, 1962), S. psammomi Mikhail et Fahmy, 1969, S. pauciproglottis Quentin, 1965, S. media Quentin, 1971, S. occidentalis Hunkeler, 1972, S. madagascariensis Quentin et Durette- Desset, 1974 (Figs. 5-13). Other species of the genus Skrjabinotaenia Akhumyan, 1946 included in this genus by GENOV and TENORA (1979) are transferred by us to the genus Meggittina Lynsdale, 1953 (Figs. 1-4).

2. Genus Meggittina Lynsdale, 19 53

Syn. : Rajotaenia Wertheim, 1954 Description: Cestodes of the family Catenotaeniidae, Skrjabinotaeniinae. Strobila a- craspedote, strongly reduced, consisting of scolex, neck and only few segments. Gravid segments not longer than wide, mostly several times wider than long. Genital pores alternat­ ing. Ovary and vitelline gland situated near to poral part of segments. Ovary highly branch­ ed, vitelline gland massive. Cirrus sac presents, is shorter than vagina. External seminal vesicle and internal seminal vesicle absent. Testes numerous, situated in two lateral groups or in two groups in front of female genital organs. Basic longitudinal stem of uterus very short, side branches not numerous, several times longer than the stem. Lateral branches giving off short wide secondary branches from their inner sides. Exact morphology of eggs unknown in type species without a pyriform apparatus. Life-cycle unknown. Parasites of rodents. Geographical distribution: Ethiopian Region, Egypt, Israel, Madagascar. Type species: Meggittina baeri Lynsdale, 1953 (Fig. 19). Deposition of "holotype: Department of Parasitology, London School of Hygiene and Tropical Medicine, London. Differential diagnosis: The genue Meggittina Lynsdale, 1953 is closely related to Skrjabinotaenia Akhumyan, 1946, differing from this genus in the formation of strobila. particularly of gravid segments, which are never longer than wide. Another significant char- acter is the formation of the uterus. Its basic stem is very short, the side branches being al­ ways several times longer than the stem. The reduction of strobila is not a characteristic feature of the genus Meggittina, since this character appears also in the species of the genus Skrjabinotaenia, On the other hand, the reduction of strobila, the formation of fully gravid segments exhibited also in their inner morphology (basic longitudinal stem of uterus very short, side branches not numerous, several times longer than the stem) may thus reflect an evolutionary character (compare in Figs 1-13), The genus Rajotaenia Wertheim, 1954 is a synonym of the genus Meggittina Lynsdale, 1953. The genus Meggittina further includes the following species: 1. M.gerbilli (Wertheim, 1954), 2. M. aegyptica (Wolfgang, 1956), 3. M. cricetomydis (Hockley, 1961).

KEY TO GENERA, SUBFAMILIES OF THE FAMILY CATENOTAENIIDAE (CATENOTAENIATA)

1. Testes situated only in lower part of proglottids, ovary always anterior to testes, genital openings in lower part of anterior third of proglottids CATENOTAENIINAE Spassky, 1949 2 Testes surrounding ovary in various ways, never only in lower part of proglottids, geni­ tal openings in upper part of anterior third of proglottids SKRJABINOTAENIINAE Genov et Tenora, 1979 5

2. Ovary symmetrical, horseshoe-shaped, vitelline gland situated posterior to ovary Quentinotaenia gen.nov. Ovary asymmetrical, vitelline gland situated near poral part of proglottis 3

3. Upper margin of ovary reaching the level of genital openings Hemicatenotaenia (Tenora, 1977) Genov et Tenora, 1979 Upper margin of ovary across the level of genital openings 4

4. Testes overlapping lateral excretory canals bilaterally Pseudocatenotaenia gen. nov. Testes not overlapping excretory canals Catenotaenia Janicki, 1904

5. Basic longitudinal stem of uterus long with numerous side branches, latter shorter than the basic stem Skrjabinotaenia Akhumyan, 1946 Basic longitudinal stem of uterus very short, only with a few side branches, latter lon­ ger than the basic stem JVIeggittina Lynsdale, 1953

HYPOTHESIS ON THE EVOLUTION OF CESTODES OF THE SUBORDER CATENOTAENIATA (Figs. 27 and 28)

According to SPASSKV (19 51), the ancestors of the Catenotaenia species belonged to primitive cestodes of the suborder Anoplocephalata. QUENTIN (1971) supposes that the Cate­ notaenia cestodes are the progeny of the Ichthyotaeniidae becoming parasites of rodents earlier than in the Oligocène. TENORA (19 76) expressed his opinion that the Catenotaenia group may be derived from cestodes parasitic in reptilians, namely from the genus Oochoris- tica. According to FREEMAN (1973), the Catenotaeniidae have common ancestors with the Protocephalidae and later derived Taeniidae. SPASSKY (1978) concluded, similarly to FREE­ MAN (1973), that the most closely related suborder to Catenotaeniata is Proteocephalata. A comparative analysis of the host and geographical distribution pictures of both Catenotaeniidae subfamilies suggests that the Catenotaeniinae are the most archaic forms. Fig. 27: Hypothetical evolution of cestodes of the suborder Catenotaeniata 50 They comprise the hosts of older paleontological appearance (Sciuromorpha: Sciuridae, He- teromyidae, Geomyidae) and are much more expanded geographically (Europe, Africa, Asia, North-America, South-America). It is reasonable to presuppose the existence of archaic Catenotaeniids parasitizing Sciuromorph rodents in the Nearctic Region already in the Oligocène (QUENTIN, 1971). They probably expanded afterwards throughout the Holarctic Region in the Miocene, parallel to the marked diversification of these rodents (see THENIUS, 1972). The remainder of these most primitive forms of cestodes are still parasitizing rodents of the Sciuromorph group both in the Palaearctic and the Nearctic Regions. These are, e. g. , Catenotaenia dendritica, known from rodents of the genus Sciurus (Sciuridae: Sciurini), C. reggiae from the genus Marmota (Sciuridae: Marmotini), or C. linsdalei from Nearctic endemic Geomyoidea (Geomyidae, Heteromyidae). These primitive forms are characterized by a large number of primary branches of uterus and a large number of testes being partially or completely divided into two groups. An impetuous development of cestodes of the suborder Catenotaeniata should have taken place in the Last Tertiary. At this time, they contact and adapt to new hosts, the . Thus, in addition to Sciuromorphic rodents, also Myomorphic ones, partic­ ularly of the families Cricetidae, Muridae, Microtidae and Gerbillidae, became infested by these parasites. Consequently, they probably began a gradual differentiation, in the general way of anatomical simplification (less number of testes and uterine main lateral branches), throughout various zoogeographical Regions. They started to penetrate, together with their hosts, from the Palaearctic to the Ethiopian Region. Not later than in the Miocene (see TENORA, 1977), the Catenotaenia spe­ cies (typical for Sciuromorph rodents) started with a new line, the genus Hemicatenotaenia, in other Sciuromorphic rodents belonging to the Afro-Asiatic Sciuridae of the tribe Xerini in Africa. Xerini appeared in the Oligocène in Europe and in the Miocene in North Africa (THENIUS, 1979). The most ancient species of this line is H. geosciuri (large number of uterine branches, tendency to divide the testes distribution into two groups, ovary not over­ lapping the level of genital pore anteriorly). Undoubtedly in the Tertiary, probably as late as in the Pliocene, the genus Pseudo­ catenotaenia was also formed. At present time, cestodes of this line parasitize only Muridae rodents of the genus Apodemus (A. sylvaticus, A. flavicollis) in the Eumediterranean region. The paleontological findings indicate that A. sylvaticus appeared in Central Europe in the Late Pleistocene and Late Holocene, perhaps deriving from other Pleistocenic forms of Apo­ demus (NIETHAMMER, 1978). The differentiation between A. sylvaticus and A. flavicollis has taken place only recently (Middle Pleistocene). The ancestors of Pseudocatenotaenia should be traced among the cestodes of the subfamily Catenotaeniinae parasitizing Myomor­ phic rodents (Muridae) in Asia, expanding posteriorly with Apodemus along the northern coast of the Mediterranean Sea. These living forms are very interesting in the sense that their outer morphology resembles the Skrjabinotaenia forms (e. g. S. lobata), whereas in the internal anatomy (number and distribution of testes) they are closely related with the Cateno­ taenia species (e. g. C. pusilla). In comparison with the data from the Palaearctic and Ethiopian Regions, the evolu­ tion of the subfamily Catenotaeniinae on the American continent was different. In the Nearctic Region, the Catenotaenia form remained stabilized tiU today without showing further changes. Only a few species of the genus Catenotaenia from this region have been reported. Three species, C. pusilla (a species with almost cosmopolitan distribution and apparently absent in Africa, the main host of which is Mus musculus) C. dentritica and Catenotaenia sp. (see RAUSCH and SCHILLER, 1948; DAVIDSON, 1976) were found in rodents of the genus Sciurus. The specific species C. reggiae was recorded in rodents of the genus Marmota. Geomyoidea mammals of the families Geomyidae and Heteromyidae are parasitized by C. linsdalei, Cri­ cetidae by C. peromysci and Microtidae by C. laguri. The last three species are sometimes wrongly regarded as synonyms of C. dendritica (see e.g. SCHAD, 1954; SMITH, 1954; WOLF­ GANG, 1956; HOCKLEY, 1961; TENORA, 1964). On the other hand, some forms from North- American rodents and described as Catenotaenia species do not belong to this genus; C. cali- fornica Powell, 1953 and C. utahensis Bienek et Grundmann, 1974. TENORA (1977) assumes that these last two species belong probably to the genus Mathevotaenia Akhumyan, 1946 (syn. Oochorictica Lühe, 1898 pro parte).

The penetration of the Catenotaeniinae in the Neotropical Region occurred only re­ cently. There is only one species known, Quentinotaenia mesovitellinica, parasitic in Cavio- morph rodents of the family Caviidae. This monotypical genus, derived from the Nearctic Catenotaenia forms, became established in South America probably in the Early Quaternary, due to the fact that South America was isolated during the whole Tertiary and a contact with the North-American fauna took place only in the Plio-Pleistocene. As pointed out already by QUENTIN (1971), Q. mesovitellinica originated probably through a capture phenomenon from Sciuridae to Caviidae, Sciurids being introduced in South America only in the Quaternary (THENIUS, 1972). The subfamily Skrjabinotaeniinae is of more recent appearance. Its origin shall be find undoubtedly in the Asiatic Palaearctic Region, probably in Myomorphic rodents of the group from the Near East. The host and geographical pictures of the Skrjabinotae­ niinae cestodes suggest that they arise in the Late Tertiary (Miocene), in connection with the migration of rodents of the families Muridae and Gerbillidae to Africa. QUENTIN (1971) sup­ poses the origin of cestodes of the genus Skrjabinotaenia from archaic Catenotaenia forms with large number of testes and small number of uterine branches. The actual remainder of such forms is Catenotaenia rhombomydis, a species parasitic in Gerbillidae from the Caspian coast (now known from the distribution area of Rhombomys opimus in the USSR). This Cate- notaenia species is morphologically similar to Skrjabinotaenia psammomi parasitic in Ger­ billidae of the genus Psammomys in Egypt. Two main evolutionary lines in Skrjabinotaeniinae can be detected. One line (genus Skrjabinotaenia) includes the historically oldest forms, all of which show the tendency to mantain the last gravid segment of strobila always longer than wide and never presenting posterior longitudinal scission. In this group it is possible to observe a gradual shortening in the length of strobila and a decrease in the number of segments through the different spe­ cies. As already noted by QUENTIN (1971), S. lobata, the longer and only species distribut­ ed simultaneously in Europe and Africa, represents the most primitive living exponent. All other species of the genus are exclusively African. The host spectrum of S. lobata allows to explain perfectly the evolution of the genus in question. This species prefers to parasitize Apodemus in Europe, only rarely infesting other rodents (Muridae, Microtidae), whereas in the Ethiopian Region (in the Palaearctic Af­ rica, southern coast of the Mediterranean Sea, there is Apodemus) it appears almost ex­ clusively in different Muridae and has been cited only sporadically in Gerbillidae. All these facts lead us to conclude that the European actual expansion of S. lobata has been reached with Apodemus coming from the Near East. An African origin of S. lobata and its posterior expansion in Europe through Gibraltar strait cannot be accepted. Pleistocenic findings of A. sylvaticus in the Atlas Mts. (North African place where A. sylvaticus shows the parasita- tion by S. lobata (MAS-COMA, FELIU and REY, unpublished data) indicate the relationship between the presence of this Murid in North Africa and its existence in the Near East (NIET­ HAMMER, 1978). As already pointed out by THALER (1973), one shall presuppose that the actual A. sylvaticus of North Africa is the result from a very recent penetration from Asia.

Fig, 28: Dispersal and differentiation of cestodes Catenotaeniata = Catenotaeniinae; = Skrjabinotaeniinae; O = Oligocenic center of dis­ persion; N = Late Neogenic center of differentiation; Q = Quaternary starting point of mi­ gration. - Catenotaenia: 1 = Sciuromorpha: Sciuridae; 2, 3, 4 = Sciuromorpha: Sciuridae, Hetero­ myidae, Geomyidae; 5 = Myomorpha: Cricetidae, Microtidae; 6 - Sciuro­ morpha: Sciuridae; 7 = Sciuromorpha; Myomorpha; 8 = Sciuromorpha: Sciuridae; Myomorpha: Muridae, Microtidae, Cricetidae. - Quentinotaenia: 5 = Cavimorpha: Caviidae. - Hemicatenotaenia: 9 = Sciuromorpha: Sciuridae: Xerini. - Pseudocatenotaenia: 10 = Mygmorpha: Muridae: Apodemus. - Skrjabinotaenia: 11 = S. lobata only: Muridae: Apodemus; Microtidae; 12 = Muroidea: Muridae, Dendromuridae, Gerbillidae, Cricetidae; 13 = S. madagascarien- sis: Cricetidae: : . - Meggittina: 14 - Gerbillidae, Muridae, Cricetidae; 15 = M. baeri: Cricetidae: Neso­ myinae: Brachyuromys. JAEGER, LOPEZ-MARTINEZ, MICHAUX and THALER (1977) has demonstrate the possibil­ ity of faunal exchanges between Europe and North Africa through Gibraltar during the Late Neogene (Miocene and Pliocene). MAS-COMA (1978) shows how Gerbillid hosts following the Betic-Rifenian-Moghrebinian archway had introduced some African helminths into Europe. Nevertheless, on the one hand Gerbillids are not usual hosts of S. lobata and have disappear­ ed today from EuFope. On the other hand, in the case that S. lobata had entered the Iberian Peninsula from the south through Gibraltar, its posterior expansion throughout Europe could not take place, since Iberian living Murids and Microtias are immigrants coming from Eu­ rope. Summing up, the most reasonable is to accept a proximal Asiatic origin for the .Skrja­ binotaenia forms, the most primitive of which, S. lobata, having started from this Near East into Europe and North Africa with Apodemus and into the Ethiopian Region with other Muroi­ dea. Subsequent introduction of primitive Skrjabinotaenia forms into the Ethiopian Region has to be continued following a gradual shortening of strobila and differentiation of species in hosts of the families GerbiUidae, Muridae, Dendromuridae and Cricetidae. The extreme case in this evolutionary line is S. pauciproglottis, evidently the shorter and youngest living form. Further differentiation inside the subfamily Skrjabinotaeniinae occurred in the Ethiopian Region. There arise another line of forms (genus Meggittina), tending to shorten and dividing longitudinally the last gravid segments of the strobila. These cestodes Skrjabino­ taeniinae are now known as parasites of African rodents of the families Cricetidae, Gerbilli­ dae and Muridae. As noted by QUENTIN (1971), already in some species of Skrjabinotaenia, such as S. psammomi and S. oranensis, it is possible to detect some signs in the last gravid segments indicating in the way of almost>«intermediate forms, near to the Meggittina mor- phology. Taking into account that both last species are parasites of Gerbillidae in North Af­ rica, QUENTIN (1971) suggest that the starting point of the Meggittina line should be in North-African Gerbillidae (the oldest Gerbillidae fossils had been found in the Late Pliocene - THENIUS, 1972), to expand to the rest of the African continent later, adapting secondarily to other families of rodents. The existence of Skrjabinotaenia madagascariensis and Meggittina baeri in Brachy­ uromys betsileoensis and B. ramirohitra (CricetidaerNesomyinae) in Madagascar give evidence that both evolutionary lines of Skrjabinotaeniinae had further spread from Africa into the Malgachian Region. As pointed out by THENIUS (1972: 180), the scarce paleontological data about Nesomyinae from the Pleistocene are not sufficient as to determine the appearance of these rodents in the island. Nevertheless, they are perhaps only "migrators" in the Late Tertiary. THENIUS (1972: 66) writes concretely: "Nesomyinae vielleicht erst im Jungtertiär eingewandert". If we accept the origin of Skrjabinotaeniinae cestodes in the Late Tertiary (Miocene), as suggested before, there had been enough time in the Late Neogene to expand throughout Africa, including Madagascar. Thus, it is not necessary to assume that the hosts of these two Malgachian cestodes were rodents which do not live anymore in Madagascar due to competition (see QUENTIN and DURETTE-DESSET, 1974: 110). CHABAUD and BRYGOO (1964), basing on MILLOT (19 52), accept also the possibility of fortuitous introductions of helminths of recent evolution through accidental transports of hosts from the African conti­ nent into the Madagascar island.

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Received: 20 January, 1980 Dr. TENORA, F. Zoological Department of the University of Agriculture CS-662 65 Brno, Zemedelská ul. 1.

Dr. MAS-COMA, S. , Dr. FELIU, C. Department of Parasitology, Faculty of Pharmacy, University of Barcelona Barcelona 28. , Spain

Dr. MURAI, É. Zoological Department of the Hungarian Natural History Museum H-1088. Budapest, Baross u. 13.