Brachylaima (Brachylaima) Sp

HIGH PARASITE BURDENS BY BRACHYLAIMA (BRACHYLAIMA) SP. (TREMATODA: BRACHYLAIMIDAE) IN TWO DOGS IN THENORTHOFSPAIN

I I 2 3 J.A. GUISANTES , A. BENITO , J.J. ESTlBALEZ & S. MAS-COMA

IDepartamento de Inmunologia, Microbiologia y Parasitologia, Facultad de Farmacia, Universidad del Pais Vasco, Apartado 450,01080 Vitoria, Spain 2Departamel11ode Sanidad y Proteccion de los Consumidores (DEMSAC), Ayuntamiento de Viroria, Calle Sail Yicente, 01001 Yitoria. Spain 3DeparramelllO de Parasitologia, Facultad de Farmacia, Universidad de Valencia, A v. Yicent Andres Estelles sin, 46100 Burjassot - Valencia, Spain

Received 20 November 1994; accepted 22 December 1994

REFERENCEG:UISANTES(l.A.), BENITO(A.), ESTIBALEZ(1.J.) & MAS-COMA(S.), 1994.- High parasite burdens by Brachylaima (Brachylaima) sp. (Trematoda: Brachylaimidae) in two dogs in the North of Spain. Research and Reviews in Parasitology, 54 (4): 255-258. ABSTRACTBr: achylaimid specimens were found in the small intestine of a male and a female greyhounds coming from a little village located in a valley in the North of Spain. The microscopical study demonstrated that all specimens belong to one species of the subgenus Brachylaima (Brachylaima) (Dujardin, 1843) Travassos et Kohn, 1964 (Brachylaiminae). It is worth mentioning the high number of specimens (a total of 180 and 55 digeneans in the male and female dogs, respectively) and their mature stage (high number of well formed eggs in the uterus), suggesting that it is a brachylaimid species perfectly able to develop in dogs. This finding is the first report of a natural infection by brachylaimid digeneans in dogs. Other reports of brachylaimids in carnivorous mammals are discussed. KEYWORDSTr: ematoda, Digenea. Brachylaimidae, Brachylaima (Brachylaima) sp., dogs, Carnivora, Spain.

INTRODUCTION (only insectivorous Soricidae) (MAS-COMA & GALLEGO, 1975). Other brachylaimids are able to deve- The family Brachylaimidae Joyeux et Foley, 1930 lop in members pertaining to different mammalian or- (Trematoda: Digenea) includes numerous species whose ders, such as Dollfusinus Biocca et Ferretti, 1958 (its definitive hosts are restricted to given animal groups: only species parasitizes insectivores of the family Erina- among mammals there are species which parasitize ceidae, as well as rodents of the families Gliridae and members of the orders Insectivora, Rodentia and Marsu- Muridae) (MAS-COMA & MONTOLlU, 1987).Finally, pialia, and among birds, brachylaimid species are found there are also species which show a large spectrum of in up to six different orders. Concerning mammals, the potential definitive hosts, as it can be found among the findings of brachylaimid species in Artiodactyla, Carni- type genus Brachylaima Dujardin, 1843 sensu lato. The vora and Lagomorpha are very rare and only sporadic, papers by KRULL (1934), BALOZET (1937), SIMON-vi. all suggesting that they cannot be considered as true de- CENTE (1955a, b) and TIMON-DAVID(1959) have experi- finitive host groups of these digeneans. This can be ex- mentally demonstrated, for given Brachylaima species, plained by taking into account that, in brachylaimids, that the adult stage of the same digenean species is able only terrestrial molluscs act as second intermediate hosts to infect and successfully develop in definitive hosts as harbouring the infective stage of metacercaria (the infec- different as species of mammals and birds. tion of the definitive host takes place through ingestion The aim of this paper is to present a new report of ma- of snails harbouring metacercariae) and that terrestrial ture specimens of a brachylaimid species in dogs, to des- snails do not constitute part of the habitual diet of the cribe the material and to discuss this very interesting fin- members of these three host groups. This fact would ex- ding. plain why brachylaimids have been unable to colonize such host groups during their evolution (VALERO, 1986). Moreover, within the family Brachylaimidae, the spe- MA TERIAL A D METHODS cificities at the level of definitive host greatly differ, de- pending on the brachylaimid genus in question. There In the necropsies of dogs for echinococcosis, a great number of are species which show a marked specificity, as in the adult trematodes were found in the small intestine of two four- month-old greyhounds, one male and one female, of the same lit- case of the genera Ityogonimus Luhe, 1899 (whose spe- ter. The dogs were from Narvaja, a little village of the province of cies infect only insectivorous mammals of the family Alava, in the North of Spain. This village (42°54'29" Nand Talpidae), Panopistus Sinitsin, 1931 (only insectivorous 1026'25"W) is at an altitude of 594 m, located in a fertile valley Soricidae) or Pseudoleucochloridium Pojmanska, 1959 called «Llanada alavesa» (ESTORNES-LASA& ESTORNES-ZUBIZA- 256 I.A. GUISANTES et al.

RRETA, 1991).The mean annual temperature is 11,3° C, and the 1964 (Brachylaiminae) (see TRAVASSOS& KOH ,1964, mean annual rainfall is 855 mm, with 58% of this rainfall occu- 1966; TRAvASSOS,TEXElRADEFREITAS& KOHN, 1969; rring during the autumn and winter (LLANOS ORTIZ-DE-LANDA- YAMAGUTI, 1971), mainly: acetabulum located in the LucE,1983). first third of the body; genital pore in the zone of the an- A total of 180 and 55 trematodes were obtained from the male and female dogs, respectively. The trematodes were stained with terior margin of the anterior testis; gonads located in the Semichon's carmine and mounted in Eukitt (0. Kindler GmbH & posterior part of the body, close together and near the Co., Germany). The study of the morphoanatomy and the measure- posterior extremity of the body; vitelline glands exten- ments of these adult digeneans was made according to the method ding from the zone anterior to the first testis to a level described by MAs-CoMA, Mo TOLlU & VALERO (1984). Drawings not surpassing the anterior margin of the acetabulum; were made with the aid of a drawing tube. uterus extending up to the intestinal bifurcation and thus clearly surpassing the anterior margin of the acetabulum. RESULTS Unfortunately, it is not possible to determine the species. As already stated by MAS-COMA & Mo TOLfU A detailed microscopical study clearly suggests that (1986) and MONTOLfU&MAS-COMA(1986), in the case all specimens belong to the same digenean species. The of species of the subgenus Brachylaima (Brachylaima) morphology of the brachylaimids found is shown in Fig. there are several species which present the same mor- 1. Extreme and mean values of their measures are given phoanatomical pattern at adult level and whose specific in Table 1. determination becomes impossible if the life cycle and The morphoanatomy allows us to include these parasi- the cercaria] chaetotaxy are unknown. The brachylaimid tes definitely within the genus Brachylaima. Moreover, species found in dogs completely fits in the pattern of se- there are several characteristics which permit this spe- veral Brachylaima (Brachylaima) species known to pa- cies to be assigned to the subgenus Brachylaima rasitize rodent hosts (see for instance MAS-COMA & (Brachylaima) (Dujardin, 1843) Travassos et Kohn, Mo TOLru, ]986).

o.srnm

Fig. 1.- Brachylaima (Brachylaima) sp. from dogs: three mature specimens in ventral view. Scale bar = 500 urn. A brachylaimid digenean in dogs in Spain 257

Characteristics (n = 11) E.V.

Lenght 1975-2300 2116 Maximum width 700-1100 851 Oral sucker 240-3401190-310 278/247 Acetabulum 240-380/230-370 296/282 Sucker ratio 0,6-1,0 0,9 Pharynx 140-2201135-180 178/155 Testis I 220-470/190-380 331/260 Testis 2 260-420/200-330 327/267 Ovary 180-300/120- 190 239/154 Eggs 16-20/25-30 28/18 Distance between suckers 170-360 250 Distance acetabulum-testis I 350-8\ 0 564 Position genital pore (anterior margin testis 2) 212-350 245

Table 1.- Morphometry of adults of Brachylaima (Brachylaima) sp. found infecting dogs. Measurements in urn. E.V.=extreme values; X =mean values; n = number of specimens studied.

DISCUSSION In Spain, specifically undetermined Brachylaima sp. adults have been found naturally infecting the intestine The most interesting aspects of this finding are: A) it of Lynx pardinus (Temminck, 1824) (Felidae) in the appears to be a brachylaimid species that is perfectly Montes de Toledo by SEGUet at. (1989), in Meles meles able to infect and develop in dogs, according to the high and Martesjoina (Erxleben, 1777) (Mustelidae) in Cata- number of specimens/host found; B) it is a brachylaimid lonia and in the north of Spain by MIQUEL (1993) and species which is able to reach maturity in dogs, accor- MOTJE (1996), in Genetta genetta (Linnaeus, 1758) (Vi- ding to the high number of well formed eggs which can verridae) from Catalonia and the northern part of Spain be distinguished in the uterus of the specimens. These by CASANOVAet at. (1992), MIQUEL (1993) and CASA- two aspects contrast with the findings of brachyaimids NOVA (1993), and also in Vulpes vulpes (Linnaeus, reported in the literature up to the present, according to 1758) (Canidae) in Catalonia by SEGOVIA(1994). It is which brachylaimds appear only very rarely and sporadi- worth mentioning here that several species of Mustelidae cally in carnivorous mammals (when detected there are have been reported among the wild fauna of the valley of only one or a very few digeneans present) and in most «Llanada alavesa» where the dogs came from: Mustela cases they appear to be immature (=non-gravid). nivalis Linnaeus, 1766; Mustela putorius jura Linnaeus, There are a very few reports on Carnivora as defini- 1758; Mustela putorius putorius Linnaeus, 1758; Mus- tive hosts of brachylaimid digeneans. In Scandinavia, tela lutreola (Linnaeus, 1761); Martes martes (Linnaeus, Brachylaima leptostomum (Olsson, 1876), which is 1758); Meles meles; Genetta genetta; and Herpestes ich- thought to be a parasite original of the hedgehog Erina- neumon widdringtoni Gray, 1842 (LLANOS ORTIZ-DE- ceus eurapaeus Linnaeus, 1758 (Insectivora: Erinacei- LANDALUCE,1983). dae), was described by OLSSON (1876) in Meles meles In all the above-mentioned findings of brachylaimids taxus (Boddaert, 1785) (Mustelidae). KRULL (1935) re- in carnivores in Spain, digeneans appear only rarely, ported that Brachylaima (Brachylaima) virginiana (Die- with very low prevalences differing according to host kerson, 1930) Dollfus, 1935, a parasite of Didelphis vir- species (i.e. 5,56, 0,99 and 2,78% in Meles meles, Mar- giniana Kerr, 1792 (Marsupialia: Didelphidae), may tes foina and Genetta genetta, respectively -see experimentally infect dogs as well as white rats, cats MIQUEL, 1993) and always showing very low burdens of and chickens, but unfortunately he did not say whether only a very few specimens per host. That is why in all the adults experimentally obtained in dogs reached ma- these papers brachyaimid infections were considered turity or not. At any rate, this report of KRULL (1935) merely as accidental, the brachylaimids in question most appears to be the only one concerning brachylaimids in probably being parasites of other hosts than Carnivora. dogs in the literature. In India, BAUGH(1962) described Owing to this and to the impossibility of specific deter- Brachylaima (Brachylaima) paradoxuri Baugh, 1962 mination, in all these papers the authors did not describe from the intestine of Paradoxurus hermaphroditus Pa- their materials. Interestingly, however, MIQUEL (1993) llas, 1777 (Viverridae). Later additional information included a whole drawing and a photograph of the concerning this digenean species to deduce whether it brachylaimid specimens he found in Genetta genetta. In really is a parasite of viverrids or another host group is these specimens of MIQUEL(loc. cit.) the vitelline glands lacking. In central Europe, STUBBE (1965) reported clearly surpass the anterior margin of the acetabulum, Brachylaima helicis (a species incertae sedis according anteriorly extending up to the level of the pharynx. This to VALERO, 1986) infecting Meles meles (Linnaeus, undoubtedly represents a brachylaimid species other 1758) (Mustelidae). than the one described here in dogs and means that there 258 I.A. GUISA TES et al. are at least two different brachylairnid species which are chez les Digenes de la famille Brachylaimidae Joyeux et Foley, able to infect carnivorous mammals in Spain. Detailed 1930. Bulletin de la Societe Neuchdteloise des Sciences Nature- descriptions of the brachylaimids parasitizing carnivores lies, 107: 185-195. are needed to determine whether there are many species MIQUEL (J.), 1993.- Contribucion al conocimiento de la helm into- fauna de los Carnivoros silvestres de Cataluiia. Tesis Doctoral, of this digenean family which are able to successfully Facultad de Farmacia, Universidad de Barcelona, Barcelona, develop in these hosts and whether there is a brachylai- 737 pp. mid which in fact uses carnivores as normal definitive MONTOUU (1.) & MAS-COMA (S.), 1986.- Una nueva problernatica hosts in its life cycle. planteada en los Digenea. Revista Iberica de Parasitologia, 46: 365-371. MOTJE(M.), 1996.- Contribucion al conocimiento de la helmintofauna de lafamilia Mustelidae (Carnivora) en la Peninsula Ibe- REFERE CES rica. Tesis Doctoral, Facultad de Farmacia, Universidad de Bar- celona, Barcelona, 472 pp. BALOZET(L.), 1937.- Brachylaemus suis Mihi, 1936, trematode de OLSSO (P.I.), 1876.- Bidrag till Skandinaviens Helminthfauna, 1. I'intestin du pore. Role pathogene et cycle evolutif. Archives de Svenska Vetensk. Akad. Handl., 14 (I): 1-35 + pI. 1-4. l'Institut Pasteur de Tunis, 26: 36-67. 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