Sci Parasitol 21(1-2):1-17, April 2020 ISSN 1582-1366 REVIEW ARTICLE

Cestodes of the genera Diplopylidium and (Eucestoda: Dipylidiiae) – a review of historical data, species inventory and geographical distribution

Rolf Karl Schuster

Central Veterinary Research Laboratory, PO Box 597, Dubai, . Correspondence: Tel. +9714 3375165, Fax +9714 33666568, Email [email protected]

Abstract. Italian parasitologists (P. Marchi of Florence, Corrado Parona of Sardinia, Vincenco Diamare of Naples, Prospero Sonsino of Pisa) of the second half of the 19th century deserved respect in the exploration on the life cycle of dipylidiid cestodes by finding and describing larval stages of these tapeworms in . They also gave the description of the strobilar stages of cestodes (Joyeuxiella echinorhynchoides, J. pasqualei and Diplopylidium acanthotetra) detected in carnivores. At the beginning of the 20th century, scientists from Spain (Carlos R. Lopez Neyra of Granada in cooperation with Jose M. Munoz Medina) and France (Charles Joyeux) proved experimentally the affiliation of larval stages from reptiles to the adult cestodes in cats. Further cestodes of the genus Diplopylidium and Joyeuxiella were described from African mammals and carnivores from India and the southern parts of the former Soviet Union. Witenberg (1932), Matevosjan (1963) and Jones (1983) reviewed the genera and reduced the number of valid species. D. acanthotetra, D. genettae, D. nölleri, D. polyacantha, D. zschokkei, D. monoophorum, J. pasqualei, J. echinorhynchoides and J. fuhrmanni were considered valid species. Of these, D. genettae, D. monoophorum, D. zschockei were not found again in recent times and the position of J. rossicum remains dubious. Other cestodes of these genera were insufficiently described or synonyms to already known species. Historical and recent findings showed that Diplopylidium and Joyeuxiella species occur in countries of southern Europe and Northern Africa surrounding the Mediterranean Sea, in the Middle East, in Central and South Asia, East and South Africa. They are no reports of the indigenous cases of these cestodes in America, Australia and northern East Asia. The life cycle of these cestodes is not fully disclosed. Larval stages of both genera were found in 60 species. Single findings of Joyeuxiella cysticercoids were also made in amphibians, rodents and insectivores.

Keywords: Joyeuxiella; Diplopylidium; Dipylidiidae; Carnivores; Reptiles.

Cestode din genurile Diplopylidium și Joyeuxiella (Eucestoda: Dipylidiiae) – o evaluare a datelor istorice, a inventarului speciilor și a distribuției geografice

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Rezumat. Parazitologii italieni (P. Marchi din Florența, Corrado Parona din Sardinia, Vincenco Diamare din Napoli, Prospero Sonsino din Pisa) din a doua jumătate a secolului al XIX-lea merită respectul pentru investigarea ciclului biologic al cestodelor dipilidiide și prin găsirea și descrierea stadiilor larvare ale acestor tenii la reptile. De asemenea, au oferit descrierea stadiilor strobilare ale cestodelor (Joyeuxiella echinorhynchoides, J. pasqualei și Diplopylidium acanthotetra) detectate la carnivore. La începutul secolului XX, oamenii de știință din Spania (Carlos R. Lopez Neyra din Granada, în cooperare cu Jose M. Munoz Medina) și Franța (Charles Joyeux) au dovedit experimental apartenența etapelor larvare de la reptile la cestode adulte la pisici. Alte cestode din genurile Diplopylidium și Joyeuxiella au fost descrise provenind de la mamifere africane și carnivore din India și din sudul fostei Uniuni Sovietice. Witenberg (1932), Matevosjan (1963) și Jones (1983) au revizuit genurile și au redus numărul de specii valabile. D. acanthotetra, D. genettae, D. nölleri, D. polyacantha, D. zschokkei, D. monoophorum, J. pasqualei, J. echinorhynchoides și J. fuhrmanni au fost considerate specii valide. Dintre acestea, D. genettae, D. monoophorum, D. zschockei nu au fost găsite din nou în vremurile recente și poziția lui J. rossicum rămâne dubioasă. Alte cestode din aceste genuri au fost insuficient descrise sau sinonime cu specii deja cunoscute. Descoperirile istorice și recente au arătat că speciile Diplopylidium și Joyeuxiella apar în țările ca sudul Europei și Africa de Nord care înconjoară Marea Mediterană, în Orientul Mijlociu, în Asia Centrală și de Sud, Est și Africa de Sud. Nu sunt raportate cazurile noi ale acestor cestozi în America, Australia și Asia de nord- est. Ciclul de viață al acestor cestode nu este dezvăluit complet. Etapele larvare ale ambelor genuri au fost găsite la 60 de specii de reptile. Descoperirile unice ale cisticercoizilor Joyeuxiella au fost, de asemenea, descoperite la amfibieni, rozătoare și insectivore.

Cuvinte cheie: Joyeuxiella; Diplopylidium; Dipylidiidae; Carnivore; Reptile. Received 29.12.2019. Accepted 12.02.2020.

Introduction Despite the wide distribution of species of the other two genera, Diplopylidium and Joyeuxiella, Dipylidium Leuckart, 1863, Diplopylidium in subtropical and tropical countries, their full life Beddard, 1913 and Joyeuxiella Fuhrmann, 1935 cycle of that includes reptiles remained nebulous of the family Dipylidiidae Railliet, 1896 are until recent times. A large number of different tapeworm genera species of which parasitize species names occurred in the literature, but the small intestines of carnivores. most of them insufficiently described, were synonyms to known species, or were never found Examination of the life cycle of Dipylidium again after the original description. Also, the caninum (Linnaeus, 1758), the type species of independent description of the larva stages in the genus Dipylidium started more than 150 reptiles and their strobilar stage in carnivores years ago when Melnikov (1869) found the caused some confusion. In addition, generic larval stage in the biting louse Trichodectes names had changed over time from Taenia to canis. Sonsino (1889a) detected cysticercoids Dipylidium, a genus that was later split into of this tapeworm in fleas and suggested that Dipylidium, Diplopylidium and Joyeuxia. Since the due to the small diameter of their mouthparts name Joyeuxia was already preoccupied adult fleas are not able to ingest the parasite Fuhrmann (1935) suggested the genus eggs and that flea larvae are the stage that are Joyeuxiella. able to swallow the cestode eggs. The whole development of D. caninum in Pulex irritans The aim of this paper is to review the discovery and Ctenocephalides canis was studied by history of Diplopylidium and Joyeuxiella species Joyeux (1920). and their geographical distribution.

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Review of the discovery history might be the larval stage of Dipylidium trinchesi, a small cestode of the cat of 25 mm The Italian parasitologist Marchi (1872)1 in length that Diamare (1892) had described detected armed cysticercoids attached to the previously4. intestinal wall of a gecko (Ascalabotes mauritanicus2). The scolex of the parasite Lopez-Neyra and Munoz Medina (1919) was armed with 70 hooks arranged in four detected the larval stage of D. trinchesii at circles. The size of the hooks ranged from 6 pleura and mesenterium of wall lizards to 18 µm. collected in Granada/Spain and compared it to C. acanthotetra of Parona. Parrot and Joyeux An inoculation trial by Marchi (1879) with (1920) proved experimentally by infection of cysticercoids found in the same host caused cats with cysticercoids from wall geckos that some confusion. The author fed the alleged C. acanthotetra is the larval stage of D. tapeworm larvae found in the viscera of a trinchesi. wall gecko to a cat, a vulture and an owl and detected six days later small worms only in Lühe (1898) described Dipylidium triseriale the intestine of the owl. It is assumed that from a genet in Tunesia. According to the Marchi dealt with a mixed infection of author, this species was morphologically very cestode larvae and cystacanths of an close to D. trinchesi and both species were acanthocephalan species and that the “small later synonymized with Diplopylidium cestodes” recorded in the gut of the owl were acanthotetra by Witenberg (1932). in reality juvenile acanthocephalans. Lopez-Neyra and Munoz Medina (1921) Rizzo (1902) reported Cysticercus recorded a further new species from cats in ascalabotidis apart from wall geckos also Granada (Spain). The length of Dipylidium from garden lizards (Lacerta agilis) from quinquecoronatum was 65 mm and its scolex Sicily without giving further morphological was furnished with five rows of rostellar details. It is assumed that this was the same hooks. According to Witenberg (1932), it was larval stage Marchi dealt with (Lopez-Neyra, identical with D. acanthotetra. D. acanthotetra 1927b). was also found in a dog in (Gnezdilov and Cebotarevic (1934). The figure • Diplopylidium acanthotetra (Parona, 1886) of the anterior end of the cestode however, showed an unusual long neck. Parona (1886) discovered Cysticercus acanthotetra, a so far unknown cestode larval • Joyeuxiella echinorhynchoides (Sonsino, 1889) stage attached to the intestinal wall of a juvenile green whipsnake (Coluber In a short note, Sonsino (1889b) reported the viridiflavus3) in Sardinia. The rostellum of this finding of Taenia echinorhynchoides in a larval stage was armed with approximately 80 fennec fox (Vulpes cerda) from . The to 90 hooks arranged in four circles. The size new cestode with two lateral genital of the hooks measured 69, 59, 33 and 18 µm. openings and a length of 7 cm seemed to be By comparing scolex structures, Diamare related to Taenia caninum and was (1894b) concluded that this cysticercoid subsequently transferred into the genus Dipylidium. The striking difference were 16 rows of 5-18 µm long hooks, on the long 1 Prior to Marchi, already Rudolphi (1819) referring to cylindrical rostellum. Since Sonsino did not communications with Bremser mentioned cestode larval stages in the body cavity of the European green and the European wall lizards. These stages possessed an unarmed scolex, were called dithyridii and are known 4 The original description by Diamare (1882) did not today as tetrathyridii, the larval stage of the cestode mention the size of the rostallar hooks, arranged in 4 genera Mesocestoides. circles. It only said that the hooks are three times bigger 2 Today Tarentola mauritanica (common wall gecko) - a than those of D. caninum and contrary to those of D. geckonid species that is widely distributed in the western caninum they were divided into root, guard and blade. A Mediterranean region. table given in a later paper (Diamare, 1894b) gave hook 3 Today: Hierophis viridiflavus. lengths for D. trinchesi of 36, 30, 22 and 12 µm.

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mention gravid segments it can be concluded chyceri and D. rossicum with J. pasqualei that the strobila was prepatent. Due to the making the former ones junior synonyms. morphological conformance Diamare (1894a) was convinced that a Cysticercoides • Diplopylidium monoophorum (Lühe, 1898) rostratus of Mingazzini (1893) could have been the larval stage of Dipylidium While studying cestodes of a zibet cat, most echinorhynchoides. The adult cestode was probably a common genet (Genetta genetta)6 also found in a fox in Tunesia (Lühe 1898) shot in the outskirts of Tunis, Lühe (1898) and later in a jackel in Mauritania (Joyeux described a cestode with a maximum length of 10 and Baer, 1930). mm. Dipylidium monoophorum had scolex structures comparable to D. triseriale with larger • Joyeuxiella pasqualei (Diamare, 1893) hooks measuring only 30 µm. The most striking difference however, were ovaries consisting only Dipylidium pasqualei, a larger cestode of a single rounded, compact lobe while ovaries measuring 20 – 30 cm in length, was described of all other species of the genus were bilobed. from a cat from Egypt by Diamare (1893). Also, the testes posterior to ovaries in the slim Apart from bigger measurements of strobila mature segments were arranged in two and scolex it differed also in the shape of the longitudinal rows. In gravid segments, genital rostellum from a similar cestode that Sonsino openings were moved forward without egg (1889) found in the fennec fox. capsules between the cirrus sacs. The description of D. monoophorum was completed by Lopez- Among numerous cestodes in the gut of a cat Neyra (1927a) and Witenberg (1932). from Hungary5 there were specimens similar to D. pasqualei that v. Ratz (1897) named • Diplopylidium zschokkei (Hungerbühler, Dipylidium chyceri. Lopez-Neyra and Munoz 1910) Medina (1919) described the subsequent larval stage in wall geckos in Granada in Spain. By Dipylidium zschockei was described by experimental inoculation of these cysts in a Hungerbühler (1910) from a yellow mongoose kitten, the authors could close the life cycle of (Cynictis penicillata) trapped in the Kalahari of this tapeworm. Also, Parrot and Joyeux (1920) South Africa. According to the description, this were able to produce the adult cestode in a cat species was close to D. triseriale of Lühe (1898) after a feeding experiment with cysticercoids but differed by a larger strobila size of 120 mm, obtained from wall geckos. a conspicuously long unsegmented neck and smaller dimensions of hooks (45, 30, 17 µm). Skrjabin (1923) described Dipylidium Joyeux (1921) found cysticercoids with scolex rossicum from a dog (out of 89 dissected) in structures matching with those of D. zschokkei the Rostov Region in Southern Russia based in a horned viper (Cerastes cornutus) in on a single specimen. Scolex structures and Northern Africa. morphology of hermaphrodite segments matched with those of D. pasqualei but gravid • Diplopylidium genettae Beddard, 1913 segments contained several eggs. It is noteworthy that the dog was also infected Beddard (1913) gave a description of two with a large number of D. caninum. According tapeworms from a common genet from London to Skrjabin (1923) D. rossicum was also found Zoological Garden. He named one species in one out of 210 dissected cats from the same Diplopylidium genettae and created a new region. genus, Diplopylidium. D. genettae consisting of 28 proglottids was 6 mm long and its rostellum After being transferred into the new genus was armed with two circles of hooks. Joyeuxia, Witenberg (1932) synonymized J. The main characters of the newly established 5 The origin of the cat was not mentioned. At that time, genus Diplopylidium were: Hungary was part of the Austria-Hungarian Empire that included also territories at the Mediterranean like 6 The author mentioned only the German name: Slovenia, Croatia, Bosnia-Herzegovina and Montenegro. Zibethkatze.

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- a retractile muscular rostellum armed with based, conical rostellum, armed with 8-12 rows two circles of hooks7; of thorn like hooks in an average size of 10 µm. - a double set of reproductive organs in each The strikingly long cirra and the coiled vasa proglottid; deferens occupying the anterior part of mature - vagina in front of cirrus sac; segments suggest that this species could have - large and muscular cirrus sac, cirrus been identical with J. fuhrmanni. coiled, slender and unarmed; - numerous testes filling available spaces in Only Witenberg (1932) cited Setti (1895) and the proglottid; Kofend (1921) and listed D. gervaisi and - ovaries in front of vitelline glands, vagina Dipylidium sp. as synonyms for J. pasqualei. narrow with a receptaculum seminis; - uterus with numerous cavities each • Diplopylidium nölleri (Skrjabin, 1924) containing a single egg only. During the 5th Russian helminthological • Joyeuxiella fuhrmanni (Baer, 1924) expedition to Russian Turkestan, Skrjabin (1924) described Progynopylidium nölleri from a cat Baer (1924) listed a number of helminths from Perowsk8. The 40 to 50 mm long dipylidiid collected by Arnold Theiler in South Africa and strobila stroke due to the dark brown given to Otto Fuhrmann. Amongst them, was a 30 pigmentation of the gravid segments. The scolex mm long cestode from a serval cat (Leptailurus was armed with three to four rows of rostellar serval Schreber, 1776) with 14 to 16 rows of rose hooks in a total number of up to 100. In thorn shaped rostellar hooks. Striking features of premature segments, female reproductive organs this new species, Dipylidium fuhrmanni, were the occur first before testes can be seen. The vagina concentration of testes in the mature segments enters the genital pore in front or ventral to the posterior to vasa deferens, the situation of genital cirrus pouch. pores in the anterior part of the segments, the presence of thin and very long cirra and single Skrjabin (1924) pointed out that Perowsk was eggs in egg capsules that are confined medially to the northernmost place for P. nölleri. In more the longitudinal excretory vessels and are southern latitudes it was found in higher concentrated in the posterior part of the gravid prevalence comparable to those of D. caninum. segments. The author suspected that Dipylidium Lopez-Neyra (1928) described Progynopylidium sp. of Kofend (1921) collected from a serval in monoophoroides – a very similar cestode with also belong to this species. However, in reddish brown terminal segments in dogs from that description the cirrus was described as Granada, Almeria and Cordoba in southern Spain. cylindrical and egg capsules were seen also P. monoophoroides differed only by a slightly externally to the longitudinal excretory vessels. larger number of testes from P. nölleri and is now treated as a junior synonym. Ortlepp (1933) recorded J. furmanni also in a domestic cat in South Africa and Hudson (1934) • Diplopylidium polyacantha Velikanov, 1982 and Mettric & Beverley-Burton (1961) described the species from serval cats in Kenya and Sharpilo (1976b) mentioned a larval stage of a Southern Rhodesia (today: Zimbabwe), Diplopylidium species with seven to ten rows of respectively. rostellar hooks in six lizard and two species in Azerbaidzan and southern Little attention was paid to a paper by Setti . In a feeding experiment of a (1895) who described Dipylidium gervaisi from a juvenile fox, a dog and a cat with Caspian gecko genet (Genetta tigrina) from . This small (Tenuidactylus caspius), Velikanov (1982) could sized tapeworm species named after the French produce the strobilar stage of Diplopylidium natural scientist Paul Gervais had a cylindrically polyacantha, a cestode of 20 to 40 mm in length. The relative large scolex of 400 to 500 µm was 7 Beddard studied histological sections of the cestode and armed with nine rows of hooks of which the in one section he saw 2 circles of hooks. Most probably he missed further circles because they were situated at a different level. 8 Perowsk is today Qysyldora in southern Kazakhstan.

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largest measured 65 – 71 µm. These hooks were cat by Shinde and Pawar (2001), D. shindei striking due to a long and thin blade. Velikanov from a dog by Chavan et al. (2003), D. (1989) mentioned eight lizard and four snake parvatiae from a cat by Shinde et al. (2004), D. species from Turkmenistan in which the larval shindei9 from an Asian palm civet stage of D. polyacantha was found. While the (Paradoxurus hermaphrodites) by Patil et al. percentage of infected lizards was small, snake (2007) and D. murtizarpurensis from a cat by species showed prevalence between 36.7 in Sawakar (2014) were wrongly allocated to the Spalerosophis diadema and 41,9% in genus Diplopylidium. In fact, they must belong Psammophis lineolatus. to the genus Joyeuxiella since drawings of the mature segments showed the position of the Description of further species vagina posterior to the cirrus sac and only the size of the rostellar hooks of D. Popov (1935) found cysticercoids in the aurangabadensis, D. shindei (by Chavan et al., peritoneum of Caspian geckos (Tenuidactylus 2003) and D. murtizarpurensis resemble those caspius) caught in Karabach/Azerbaidzan. of Diplopylidium. Only D. chandensis from Cysticercoids contained in cysts of a size of 800 jungle cat (Felis chaus) described by µm had a rostellum with four rows of hooks Suryawanshi et al. (2010) matched with (42, 19, 12, 7 µm). A feeding experiment with features of the genus Diplopylidium. All “new” two cats revealed six weeks after inoculation species from India have never been findings of three cestodes in the small intestine mentioned in the literature again. of one cat. The size of the cestodes varied between 4 and 5 cm and scolex structures and species inventary matched with those of the cysticercoids. The helminth was named Diplopylidium skrjabini. The name Dipylidium was created by Leuckart The adult cestode was nearly identical with D. (1863) for cestodes with two marginalized noelleri and differed mainly in a shorter length genital openings in which male and female of rostellar hooks of the 2nd row. The species genital ducts lead. The rostellum of these has never been reported again. cestodes is armed with multiple rows of small hooks which have a disc shaped root. Gravid A number of Diplopylidium and Joyeuxiella segments contain eggs glued together as larger species were reported from India. Amongst conglomerates. Despite the new name, the them was J. pasqualei in domestic cats and in a author called the tapeworm that occurs wild cat in Dehli by Gill (1972) and Das et al. frequently in dogs and cats Taenia cucumerina, (2011), respectively. In addition, Agrawal and with synonyms T. elliptica and T. canina. For Pande (1980) found cysticercoids in a yellow the first time, Diamare (1892) used Dipylidium bellied gecko (Hemidactylus viridiflavus) and as genus name and gave a definition. Contrary were able to raise the strobilar stage of J. to Leuckard, Diamare defined egg capsules in pasqualei in an experimentally infected cat. gravid segments to contain one or several eggs.

Capoor and Srivastava (1976) found a large In a monograph on the old genus Dipylidium, number of J. vulpusi in a fox in Allahabad. The Diamare (1894b) recognized D. caninum, D. description of J. vulpusi however, matched trinchesi, D. pasqualei and D. echinorhynchoides with the redescription of J. echinorhynchoides as valid species. He considered D. genettae10 by Jones (1983) who compared material (Gervais, 1847) and D. monticellii (Diamare, collected from carnivores from South Africa, 1893) as insufficiently described but probably Palestine, , Kuwait and . Deshmukh also belonging to the genus Dipylidium and also (1990) described J. domestica from a cat. The listed all the 12 synonyms of D. caninum. descriptions of other species from India were parsimonious with missing important details like total size and the description of the gravid 9 Patil et al. 2007 did not cite the paper the paper of Chavan et al. (2003) and thus, did not know that the segments. D. udgirensis from a cat by Shinde et species name D. shindei was already preoccupied. al. (1994), D. iayashreeae from dog by Patil 10 In the very superficial original description by Gervais and Shinde (1997), D. aurangabadensis from a (1847) the cestode was named Halysis genettae. Diesing (1850) mentioned it as Taenia genettae.

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Railliet (1896) suggested some modifications considered D. caninum as the only exactly in the nomenclature of parasites within the described valid species of the genus Dipylidium. family Taeniadae11. In this connection, he The adult cestode infects canids, hyenas, cats, suggested to rename the subfamily civet cats and occasionally man. Fleas and Cystoidotaeniae and proposed the name biting lice are intermediate hosts. Dipylidiinae12 for small cestodes with two or multiple circles of rostellar hooks. These The author mentioned also D. buencaminoi cestodes have cysticercoid type larval stages. Tubangui, 1925 from a dog on the Philippines, The definition of this subfamily was later on but this species differs only by its smaller total emended, became more defined and was size and unusually smaller eggs. upgraded to family level (Matevosjan, 1953; Jones, 1983; Mariaux et al., 2017). With regards to the genus Joyeuxia he left only two species, J. pasqualei and J. echinorhynchoides. At the end of the 1920th of last century the Both differ in the number of rows of rostellar genus Dipylidium contained about 30 species of hooks 14-18 vs. 23-25)13 and the distribution of which only 18 names were more or less well eggs in the gravid segments. Due to the very known. Lopez-Neyra (1927a) discussed the much contracted holotype specimen of J. various morphological types within this genus fuhrmanni Witenberg doubted that this species is and proposed a division into three distinct substantially different from J. pasqualei, genera: especially because the scolex structures were similar. Witenberg also synonymized Dipylidium - Dipylidium: rostellar hooks rose thorn rossicum that Skrjabin (1923) described from a shaped, male genital opening in front of vagina, dog from the Don Region of Russia with J. multiple eggs in one capsule, genital openings pasqualei. posterior to middle of the segment. Type species: D. caninum. Within the genus Diplopylidium Witenberg - Joyeuxia: rostellar hooks rose thorn (1932) recognized D. acanthotetra, D. nölleri, D. shaped, male genital opening in front of vagina, zschokkei and D. monoophorum as valid species. single eggs in one capsule, genital openings in D. genettae as the type species of the genus was the middle of the segment. Type species: J. only poorly described. Only the position of the chyceri (= J. pasqualei). vagina anteriorly to the cirrus and the taenioid - Diplopylidium: part of rostellar hooks of shape of the rostellar hooks defined its taenioid type, male genital opening posterior to systematic position. D. arvicola and D. columbae vagina, genital openings in the first half of the found as strobilar stages in unusual hosts (rodent segment, one egg per egg capsule. Type and pigeon) were considered as insufficiently species: D. genettae. described.

Since the type species of Diplopylidium, D. In a short note, Fuhrmann (1935) informed that genettae, was only poorly described Lopez- the genus name Joyeuxia was already Neyra (1928) suggested to rename this genus preoccupied by a sponge and for this reason he in Progynopylidium with a properly described proposed the name Joyeuxiella. by Skrjabin (1924) type species P. nölleri. Matevosjan (1963) added D. skrjabini to the Witenberg (1932) adopted the system genus Diplopylidium. Based on a redecription of J. suggested by Lopez-Neyra (1927a, 1928) but rossicum by Gamcemlidze (1939) he also disagreed regarding the genus name restored the status of this species. Despite Progynopylidium. In his revision of the morphological similarities of J. rossicum and J. inventory of the family Dipylidiinae he pasqualei, both are listed as valid species together with J. echinorhynchoides in Fauna Europea (2019). 11 Today: Taeniidae. 12 In many sources Stiles (1896) is named as author for Dipylidiinae. However, the paper by Railliet (1896) on 13 The number of rostellar hooks reported by earlier Dipyliinae was published in March 1896 while that by scientist were counted in a wrong way resulting in lower Stiles appeared four months later. numbers.

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Jones (1983) revised the genus Joyeuxiella and Russia. Kozlov (1977) listed also J. rossicum with recognized J. pasqualei and J. echinorhynchoides, findings made in domestic and wild cats, wolves and after studying material from Onderstepoort and red foxes in Moldova, Ukraine, , Veterinary Institute, also J. fuhrmanni as valid Kazakhstan and Lower Volga region and west species. Siberia of Russia. Sharpilo (1976b) listed findings of larval stages of D. acanthotetra and Geographical distribution D. nölleri in reptiles in Turkmenistan and Uzbekistan and those of J. echinorhynchoides in Early findings of larval stages and adult cestodes Azerbaijan, Turkmenistan and Uzbekistan. were made in countries surrounding the Mediterranean. Diplopylidium acanthotetra Table 1 and Table 2 summarizes recent findings (synonyms: Dipylidium trinchesi, D. of J. pasqualei and J. echinorhynchoides and D. quinquecoronatum, D. triseriale) was reported nölleri and D. acanthotetra findings in carnivores from Italy, Spain, , Tunisia and Palestine. around the world. A further species, J. fuhrmanni, Diplopylidium nölleri (synonym: D. was mentioned in the past 30 years only in three monoophoroides) was discovered in Kazakhstan reports. Baker et al. (1989) detected the parasite and later detected also in Spain, Egypt and in 38 (=2.5%) out of 1,502 cats in Transvaal/ Palestine. The larval stage, Cysticercus rostratus, South Africa. Outside of Africa, J. fuhrmanni was of Joyeuxiella echinorhynchoides was found for found in Dubai in 30 (=12.5) out of 240 cats the first time in Italy, while its strobilar stage (Schuster et al., 2009). In a controlled test with was described from a fennec fox from Egypt. It naturally tapeworm infected cats carried out in was later also detected in Tunisia, Mauritania, Dubai 11 out of 13 were positive for J. Niger and Palestine. fuhrmanni (Schuster et al., 2016). It is notable that other species (J. rossicum, D. skrjabini, D. Joyeuxiella pasqualei (synonyms: Dipylidium monoophorum and D. gervaisi D. zschokkei) were chyceri, Dipylidium rossicum, Joyeuxia aegyptica, not reported in the past 30 years. Joyeuxia pasqualeiformis) occurred in Spain, Algeria, Egypt and was found also in Hungary, Cestodes of both genera were not always Russia, India, southern China, Malaysia, identified to species level like in the case of El Tanzania and South Africa. Shehabi (1999) in dogs and foxes and Al-Qaoud et al. (2003) in dogs in ; Zare-Bidaki et al. According to historical sources, some species, (2010) in foxes and Parsa et al. (2014) in dogs in like Joyeuxiella fuhrmanni. Diplopylidium Iran and El-Dakhly et al. (2017) in cats in Egypt. zschokkei and D. monoophorum were known The reason for this is a difficult differentiation only from Africa. The type species of the genus between the species, particularly between J. Diplopylidium, D. genettae, is poorly described. It pasqualei and J. fuhrmanni in the case of fresh was found in a genet of the London Zoological infections or, when dealing with faecal samples Garden. The origin of the host was Africa only. In addition to Tab.1, there was a case without specification of the country. report of an intestinal pleating in a cat associated with J. pasqualei infection in Greece The occurrence of strobilar Diplopylidium and (Papazoglou et al. 2006). In Corsica a J. Joyeuxiella stages in the former Soviet Union in echinorhyncoides infection was detected in a the 1950th and 1970th is well documented by road killed fox (Jordi et al., 2005). In the Kozlov (1977). According to the author, D. Lefkosia, Lemesos, Larnaka, Pafos and acanthotetra and D. nölleri were found in Ammochostos districts of Cyprus, 7% out of 185 Turkmenistan in domestic cats and in examined cats were diagnosed with Joyeuxiella Azerbaijan, Uzbekistan, Turkmenistan and and Diplopylidium infections without further Kazakhstan, respectively in in domestic and differentiation (Diakou et al., 2017). wild cats (Felis margarita, F. chaus), dogs, wolves and foxes. J. echinorhynchoides was Very few findings these cestodes were reported diagnosed in foxes in Georgia, Uzbekistan and from central Europe. In a parasitological study and J. pasqualei was diagnosed in on parasites of dogs and cats in Austria, two out Georgia, Uzbekistan, Kazakhstan and southern of 505 dissected cats were positive for J.

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pasqualei Supperer and Hinaidy (1986). only 0.1% contained Joyeuxiella/Diplopylidium Schuster and Montag (2000) reported a case of segments and none of the 3167 cat faeces were J. pasqualei in a cat in Berlin. Out of 8,438 dog positive for these cestodes (Barutzki & Schaper, faecal samples examined in southern Germany, 2003).

Table 1. Recent findings of J. pasqualei and J. echinorhynchoides in carnivores

Prevalence (%) Number Country Region Host Reference examined J. pasqualei J. echinorhynch

mid Ebro valley cat 58 29.3 Calvete et al. (1998)

All over red fox 399 2.8 6.0 Segovia Arias et al. (2004) Sierra Morena cat 19 21.0 Millan & Casanova (2007) Spain Mallorca cat 58 76.0 Millan & Casanova (2009)

Valencia red fox 286 27.6 Sanchis Monsonis (2015)

Murcia red fox 55 34.6 Martinez Carracao et al. (2007) Portugal Lisbon cat 162 16.4 Waab et al. (2014)

all over cat 1150 1.2 Symeonidou et al. (2018) Greece Tessaloniki cat 118 10.2 Gianelli et al. (2017)

Albania Tirana cat 18 11.1 Knaus et al. (2011)

Hatay dog 60 8.3 Aydenizoz (1997)

Turkey Hatay cat 8 50.0 Yaman et al. (2006)

Ankara cat 43 2.7 Öter et al. (2011)

Saudi n.i. red fox 8 6/8 Alagali et al. (2011) Arabia Kuwait city cat 103 61.2 Abdul-Salam & Baker (1990) Kuwait Kuwait city cat 240 38.3 El Azazy et al. (2016)

Babylon cat 57 12.5-20 AL-Rammahi et al. (2014) Iraq Baghdad cat 254 58.3 Al-Rubaie et al. (2015)

UAE Dubai cat 240 67.1 Schuster et al. (2009)

Tehran cat 102 3.9 Dalimi et al. (1996)

wolf 10 20.0

dog 70 11.4 Kashan Arbabi et al. (2004) red fox 22 6.0

jackal 40 7.5

Mashad dog 100 1.0 Razmi et al. (2006)

fox 22 27.3 Iran Kordestan Dalimi et al. (2006) jackal 10 30

Bandar Anzali cat 50 10 Changizi et al. (2007)

Zanjan cat 100 55 Esmaeilzadeh et al. (2009)

Kashan cat 113 85.0 Arbabi & Hooshyar (2009)

all over fox 37 10.8 Meshgi et al. (2009)

Mashad cat 52 17.6 Borji et al. (2011)

Chaharmahal dog 49 26.5 Nabavi et al. (2014)

India Puducherry cat 1 1/1 Das et al. (2011)

S. Africa Gauteng cat 1502 6.0 Minnaar & Krecek (2001)

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Table 2. Recent findings of D. noelleri and D. acanthotetra in carnivores

Prevalence (%) Number Country Region Host References examined D. nölleri D. acanthotetra

mid Ebro valley cat 58 8.6 20.7 Calvete et al. (1998) Spain All over red fox 399 0.2 Segovia Arias et al. (2004)

Mallorca cat 58 60.0 Milan & Casanova (2009)

Portugal Lisbon cat 162 3.7 Waab et al. (2014)

not indicated jackal 31 16.0 Lahmar et al. (2014) Tuenesia Ariana dog 271 27.7 Lahmar et al. (2017)

Egypt Beni-Suif cat 62 22.5 8.0 El-Dakhly et al. (2017) not indicated red fox 8 (4/8) Alagali et al. (2011)

cat 103 4.9 Abdul-Salam & Baker (1990) Kuwait Kuwait-city cat 240 54.6 45.4 El Azazy et al. (2016) Babylon (urban) 32 8.0 cat AL-Rammahi et al. (2014) Iraq Babylon (rural) 25 14.0

Babylon cat 254 50.8 Al-Rubaie et al. (2015)

Qatar Doha cat 658 47.1 Abu-Madi et al. (2010)

UAE Dubai cat 240 37.1 Schuster et al. (2009)

Tehran cat 102 37.25 Dalimi et al. (1996)

Kordestan fox 22 4.5 Dalimi et al. (2006)

Bandar e Anzali cat 50 54.0 Changizi et al. (2007)

Iran Zanjan cat 100 23.0 41.0 Esmaeilzadeh et al. (2009) Kashan cat 113 64.6 Mohsen & Hossain (2009)

red fox 37 8.1 not indicated Meshgi et al. (2009) jackal 79 5.0

Uzbekistan Samarkand dog 28 7.1 Yong et al. (2019)

The only known case of a Joyeuxiella infection (1920), 20% of the wall geckos in Algeria were in America was reported from a cat that had infected with these cysticercoids. been imported from Saudi Arabia (Blagburn & Todd (1986). For Spain, Lopez-Neyra (1927b) gave cysticercoid prevalences in wall geckos with Studies of the life cycle different cysticercoids between 6 and 25 %. These small lizards are a frequent pray of cats The involvement of reptiles in the life cycles of while are less likely to be eaten by cats. Diplopylidium and Joyeuxiella species is known In Turkmenistan, Velikanov (1989) examined for a long time. Early communications more than 1000 reptiles belonging to 34 mentioned wall lizards and whipsnakes as species and detected cysticercoids of D. intermediate hosts. The larval stages of acanthotetra in one, D. nölleri in 9, D. dipylidiid cestodes were frequently found in polyacantha in 12 and J. echinorhynchoides in lizards in Spain, Morocco, Algeria, Tunesia and 20 reptile hosts. Greece but also in snakes in southern Europe and northern Africa (Lopez-Neyra, 1927b). Snakes always showed higher prevalence Working in Palestine on dipylidiid cestodes compared to lizards. Table 3 listed 57 known Witenberg (1932) added more reptile species reptile species that are involved in the life as intermediate hosts. According to Joyeux cycles of dipylidiid cestodes.

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Table 3. Carnivore and reptile hosts of Joyeuxiella and Diplopylidium species according to Witenberg (1932), Markov et al. (1970), Radchenko (1973), Dollfus, 1975, Sharpilo (1976b), Velikanov (1982), Simonsen & Sarda (1985) and Martin & Roca (2005)

Cestode species Final hosts Reptile host

Lacerta viridis, L. muralis, Tarentola mauritanica, Hemidactylys turcicus, H. mabouia, Acanthodactylus schreiberi, Trapeolus ruderatus, Stellagama domestic cat dog, stellio, Paralaudakia caucasia, Trapelus sanguinolentus, Phrynocephalus J. pasqualei wolf, serval raddei, P. reticulatus, P. horvathi, Eremias persica, E. velox, E. grammica, E. strauchi, E. afghanistanica, Eryx tataricus, rhodorachis, P. najadum, Hierophis viridiflavus, Echis carinatus, Gloidiscus halys Acanthodactylus erythraeus, Ptyodactylus hasselquisti, Tenuidactylus caspius, Teratoscincus scincus, Crossobamom eversmanni, Asophylax pipiens, Gymnodactylus russovi, Paralaudakia caucasia, P. erythrogastra, Stellagama domestic cat dog, stellio, Trapelus sanguinolentus, Phrynocephalus horvathi, P. mystaceus, J. echinorhynchoides red fox, Varanus griseus, Eremias velox, E. intermedia, Scincus scincus, Chalcides

fennec, jackal, chalcides, Eryx miliaris, Psammophis sibilans, P. lineolatus, Hierophis viridiflavus, Boiga trigonata, Platyceps karelini, P. najadum, Hemorrhois ravergieri, H. numifer, Rhagerhis moilensis, Macrovipera lebetina, Echis carinatus, Gloydius halys Lacerta agilis, L. muralis, Gallotia atlantica, Tarentola mauritanica, domestic cat, Tenuidactylus caspius, Teratoscincus scincus, Stellagama stellio, D. acanthotetra African civet cat, Hemidactylus turcicus, Chalcides ocellatus, C. chalcides, Hemorrhois common genet ravergieri, H. hippocrepis, Hierophis viridiflavus, Malpolon insignitus, Natrix maura, Clorophis irregularis, Echis carinatus, Lacerta laevis, Tarentola mauritanica, Hemidactylus turcicus, H. mabouia, Teratoscincus scincus, Crossobamom eversmanni, Tenuidactylus fedtschenkoi, Phrynocephalus heliopscopus, Trapelus sanguinolentus, Paralaudakis domestic cat, red D. noelleri caucasica, Eremias persica, Eryx miliaris, Boiga trigonata, Platyceps fox, dog rhodorachis, P. karelini, P. najadum Hemorrhois ravergieri, H. hippocrepis, Hierophis viridiflavus, Psammophis sibilans, Malpolon insignitus, Echis carinatus, Cerastes cornutus, Macrovipera lebetina Tenuidactylus caspius, Teratoscincus scincus, Crossobamom eversmanni, domestic cat, sand Asophylax pipiens, Gymnodactylus russovi. Trapelus sanguinolentus, D. polyaqcantha cat, jungle cat, red Phrynocephalus helioscopus, P. guttatus, P. mystaceus, Eremias velox, E.

fox, dog intermedia, Eryx miliaris, Natrix testella, Platyceps karelini, Spalerosophis diadema, Psammophis lineolatus, Gloidiscus halys

The description of the larval stages was Little is known about the participation of based on microscopic examination of the other vertebrate classes in the life cycle of whole cyst or examination of the isolated these cestodes. Bursey and Goldberg (2004) metacestode. Valkounova (1982) did reported findings of Joyeuxiella sp. in Palau histological examination of D. noelleri larval frogs (Cornufer pelewensis) and Mashaii stages collected from an Egyptian cat snake (2005) detected D. acanthotetra cysticercoids (Telescoptus obtusus) caught in a village next in a green toad (Bufo viridis) in Iran. Schulz to Giza/Egypt by Rysavy (1973). The (1929) and Gamcemlidze (1939) found metacestode was surrounded by a host Joyeuxiella larval stages in the lesser white derived capsule consisting of muscles and toothed shrew (Crocidura suaveolens) in connective fiber tissue. Gelatinous matter Kazakhstan and Georgia, respectively. The filled the space between parasite and authors were convinced dealing with J. capsule. Contrary to the larval stage of D. rossicum. For this reason, further findings of caninum for which Cervi (2002) proposed the Joyeuxiella cysticercoids in small mammals name cryptocysticercus histological sections were all attributed to J. rossicum. Thus, with D. noelleri larvae did not reveal any Semenova (1968), Sharpilo (1976a) and signs of scolex invagination and no Tarasovskaja (1994) reported J. rossicum in attachment of the larva to the capsule could rodents in the lower Volga region of Russia, be observed. in Kiev (Ukraine) and in Kirgistan,

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respectively. Behnke et al. (2004) found the References larval stage of J. rossicum14 in a spiny mouse (Acomys dimidiatus) in Egypt. Abdul-Salam J., Baker M.K. 1990. Prevalence of intestinal helminths in stray cats in Kuwait. The question how reptiles become infected Vet. J. 10:17-21. with subsequent cysticercoids remained Abu-Madi M.A., Behnke J.M., Prabhaker K.S., Al- obscure. After unsuccessful inoculation Ibrahim R. Lewis J.W. 2010. Intestinal helminths of feral cat population from urban and suburban experiments of wall geckos with cestode districts of Qatar. Vet. Parasitol. 168(3-4):284- segments carried out by Joyeux (1923), the 292. author suggested that a further host is Agrawal R.D., Pande B.P. 1980. Cysticercoid of necessary and this could be a coprophagic Joyeuxiella pasqualei in the wall-lizard and its . According to Lopez-Neyra (1927c) experimental development in kitten. Indian J. house flies might play a role at least as Helminthol. 31:75-80. disseminators for dipylidiid eggs. Alagaili A.N., Mohammed O.B., Omer S.A. 2011. Gastrointestinal parasites and their prevalence in In short communication, Dadaev et al. (2005) the Arabian red fox (Vulpes vulpes arabica) from reported findings of cysticercoids in darkling the Kingdom of Saudi Arabia. Vet. Parasitol. 180:336-339. of the genus in Uzbekistan. Al-Qaoud K.M., Abdel-Hafez S.K., Craig P.S. 2003. The cysticercoids in a size of 280 – 380 µm Canine echinococcosis in northern Jordan: were embedded in connective tissue capsules increased prevalence and dominance of and were characterized by tree rows of sheep/dog strain. Parasitol. Res. 90:187-191. rostellar hooks. The hooks in the first row Al-Rammahi H.M., Safa M.K., Hammadi A.K. 2014. measured 30-40 µm, others were Prevalence of intestinal helmintes in feral cats in considerably smaller. Isolated cysticercoids Babylon province/Iraq, urban and rural transferred in jelly capsules and were orally locations. Mirror Res. Vet. 3:44-51. inoculated to four different lizards (Eremias Al-Rubaie A.-R.L., Mhaisen F.T., Al-Tae A.-R.A. 2015. velor Pallas, 1771, Trapelus sanguinoletus Survey of some gastrointestinal cestodes and nematodes from stray cats at Baghdad city, Iraq. Cuvier, 1817, Phrynocephalus helioscopus Am. J. Biol. Life Sci. 3:246-253. Pallas, 1771, Tenuidactylus fedtschenkoi Arbabi M., Doroudgar A., Hoshyar H., Mobedi I. 2004. Strauch, 1887). All these reptiles were A survey of cestode infections of carnivores in harbored cysticercoids when being dissected the Kashar region. Journal of the Faculty of 64-97 d after inoculation. The authors were Veterinary Medicine, Tehran University 59: 289- convinced to have dealt with Diplopylidium 293. noelleri. Arbabi M., Hooshyar H. 2009. Gastrointestinal parasites of stray cats in Kashan, Iran. Tropical Acknowledgements Biomedicine 26:16-22. Aydenizoz M. 1997. Konya Yöresi köpeklerindehelmintolojik arastimalar The author is grateful to Prof. Dr. V. Helminthological investigations of dogs in Konya Charchenko (Schmalhausen Institue of province [in Turkish]. Acta Parasitol. Turcica 2: Zoology, Kiev/ Ukraine), to Prof. Dr. S. 429-434. Rehbein (Boehringer-Ingelheim, Rohrdorf/ Baer J.-G. 1924. Contribution a la faune Germany) and to Dr. B. Neuhaus helminthologique Sud-Africaine. Ann. Parasitol. (Naturkundemuseum Berlin/ Germany) for 2:239-247. their help in acquisition of some historical Baker M.K., Lange L., Vester A., van der Plaat S. 1989. literature sources. A survey of helminths in domestic cats in the Pretoria area of Transvaal. Part 1: The prevalence and comparison of burdens of helminths in adult and juvenile cats. J. South Afr. Vet. Assoc 60:139-142. 14 The authors were uncertain about the species affiliation. They used the name J. rossicum since other Barutzki D., Schaper R. 2003. Endoparasites in dogs Joyeuxiella species that were known to occur in Egypt and cats in Germany 1999-2002. Parasitol. Res. employ reptiles in their life cycle. Also they cited 90:147-149. literature from Kirgistan where J. rossicum was found in Beddard F.E. 1913. Contributions to the Anatomy and rodents. Systematic arrangement of the Cestoidea. 10. On

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