Research and Reviews in Parasitology, 52 (3-4): 117-120 (1992) Editorial Fomalba, S.A. © 1993 Asociaci6n'de Parasit61ogos Espattoles ' Printed in

A SURVEY OF GLYCYPHAGID MITES PARASITIZING SMALL MAMMALS IN GALl CIA (NW SPAIN)

A. PEREIRA & J. CASTRO Seccion de Parasitologia, Departamento de Microbiologic y Parasitologia, Facultad de Farmacia, Universidad de de Compostela, 15700 , Spain

Received 18 February 1992; accepted 9 June 1992

REFERE eE: PEREIRA(A.) & CASTRO(1.), 1992.- A survey of Glycyphagid mites parasitizing small mammals in ( W Spain). Research and Reviews in Parasitology, 52 (3-4): 117-120. ABSfRAcr: A total of 620 small mammals (rodents, insectivores and chiropterans) captured in Galicia (NW Spain) was examined. Five mite species of the family Glycyphagidae were identified: Glycyphagus (Myacarus) hypudaei, Labidophorus talpae, Orycteroxenus dispar, Oryctero- xenus soricis and Xenoryctes krameri. Specimens of a species of the genus Grammolichus which could not be determined were also found. The infections of Talpa occidentalis by Labidophorus talpae and of Crocidura suaveolens by Xenoryctes krameri are reported for the first time. KEY WORDS: Acarina, Glycyphagidae, small mammals, Galicia, NW Spain.

INTRODUCTION following: Order Actinotrichida Van der Hammen 1972, Suborder Acaridida Krantz, 1978, Family Glycyphagidae Continuing our studies of small mammal ectoparasites Berlese, 1887, Subfamily Labidophorinae Zachvatkin, in Galicia, the present paper reports results with respect 1941, Genus Glycyphagus Hering, 1838, Subgenus to the glycyphagids, To date the only information about Myacarus Zachvatkin, 1941: G. (M.) hypudaei (Koch, this type of mites in Spain has been limited to the Nor- 1841); Genus Labidophorus Kramer, 1877: L. talpae theast of the country. The first reports were published by Kramer, 1877; Genus Orycteroxenus Zachvatkin, 1941:0. LUKOSCHUS(1967) and FAIN (1969 a) and referred respec- tively to Lophuromyopus apodemi Fain, 1975 (infecting Apodemus sylvaticus in Jaca) and Dermacarus hypudaei Oudemans, 1915 [infecting Microtus (Pitymys) duodecim- costatus, also in Jaca]. In recent years a more comprehen- sive understanding of the glycyphagids has developed, thanks to studies including GALLEGO& PORTUS(1982, 1987), GALLEGO,PORTUS& GALLEGO(1983, 1988), POR- TUS& FAIN (1982) and PORTUS,ESPONERA& GALLEGO (1987).

MATERIAL AND METHODS

Sampling was carried out in 40 districts throughout the four pro- vinces of Galicia (Fig. I). A total of 620 small mammals of 15 species was collected (Table I). Removal of parasites from hosts and subsequent counting and mounting was carried out according to standard procedures (PEREIRA-LoRENZO, COUCE-CANEIRO & QUINTEIRO-Aw so, 1987). For the identification of glycyphagids the criteria of FAI (1969 a, pers. comm. 1991) were followed.

RESULTS ORENSE

Fig. 1.- Localities of the four Galician provinces where the hosts Of the 620 small mammals examined, 160 were were collected: La Coruna: I) Ames; 2) Bri6n; 3) ; 4) Car- parasitized by glycyphagids: the overall infection ballo; 5) ; 6) ; 7) Curtis; 8) ; 9) La Co- prevalence was thus 25,81 0,10. Table 1 shows prevalence runa; 10) Oleiros; 11) 0 Pino; 12) Padr6n; 13) Rois; 14) Santiago; and intensity for each of the host species captured, 15) Teo; 16) . Lugo: I) Alfoz; 2) Antas de Ulla; 3) Lugo; Five species of glycyphagid plus one member of the 4) Monforte de Lemos; 5) Monterroso; 6) 0 Caurel; 7) Paradela. genus Grammolichus were identified, The distribution of Orense: I) Cartelle; 2) Larouco; 3) Laza; 4) 0 Bolo; 5) Orense; 6) Puebla de Trives; 7) Villamarfn; 8) Vilarino de Couso. Pontevedra: these taxa in relation to the various host species, with I) Cangas de Morrazo; 2) Covelo; 3) Nigran; 4) 0 Grove; 5) prevalence in brackets, is shown in Tables 2 and 3. Ponteareas; 6) Salvaterra do Mino; 7) Valga; 8) Vigo; 9) Vila de The systematic position of the species found is the Cruces. 118 A. PEREIRA & J. CASTRO dispar (Michael, 1886), 0. soricis (Oudemans, 1915);Sub- sy/vaticus, although its presence on the latter species may family Lophuromyopinae Fain, 1967, Genus Xenoryctes be considered accidental. Zachvatkin, 1941: X krameri (Michael, 1886); Genus Concerning 0. soricis, HAITLlNGER(1977) states that Grammo/ichus Fain, 1968: Grammo/ichus sp. it occurs principally on insectivores and only rarely on rodents, whilst GALLEGO, PORTUS& GALLEGO (1988) claims that the species is not only specific to soricids bur DISCUSSION that it is also limited to humid-zone hosts (Neomys fo- diens, S. araneus, S. coronatus and S. minutus) and totally G. (M.) hypudaei is a highly adaptable species absent from drier-zone hosts (such as Crocidura russu/a). (GALLEGO,PORTUS& GALLEGO, 1988), infecting both Like HAITLlNGER(1977), GALLEGO,PORTUS& GALLEGO rodent and insectivore hosts. We found it on 120 of the (1988) consider this species to occur only accidentally on 620 host specimens examined (Tables 2 and 3). It has been rodents. In spite of all the above, we found this species previously cited in Spain by various authors (FAIN & infecting 7 Apodemus sy/vaticus individuals captured in LUKOSCHUS,1974; GALLEGO & PORTUS, 1982, 1987; two different districts and with a mean infection intensi- GALLEGO, PORTUS & GALLEGO, 1983; PORTUS, ty of 5 parasites (min. 1, max. 19) per host; we do not ESPONERA& GALLEGO, 1987). consider these data indicative of accidental infection. L. ta/pae is a common insectivore parasite, typical of Equally, we found this mite on 3 of the 33 C. russu/a ex- Ta/pa europaea and Sorex minutus (GALLEGO, PORTUS amined, with a mean infection intensity of 270 parasites & GALLEGO,1988). We collected it from Ta/pa occiden- (min. 1, max. 800) per host. ta/is, this being the first time that this species has been Our results confirm the opinion of GALLEGO,PORTUS reported on this host. & GALLEGO(1988) that X krameri is a euryxenic species, 0. dispar is one of the few glycyphagids whose life cy- found on both insectivores and rodents. We report for the cle is fully understood (FAIN, 1969 b). It has been first time the infection of Crocidura suaveo/ens by this reported as a habitual parasite of Ta/pa europaea in several species. European countries (FAI ,1969 a). This author has also The genus Grammolichus was created by FAl (1968 found the species infecting Ta/pa caeca (= Ta/pa occiden- a) to include six species of glycyphagid mites occurring ta/is), Microtus arva/is and Dasymys incomtus rufu/us. as parasites of various African rodents and birds. The We found it on six Ta/pa occidenta/is and one Apodemus study of the life cycle of one of these species led the same

Total Prevalence Intensity of Hosts Captured Parasitized Glycyphagids (070) parasitation x (min.-max.)

Rodentia

Asy 354 120 2627 33,89 21,89 (I-800) Mag 2 I I 50 I (I-I) Mdo 135 9 171 6,66 19 (1-128) Rra 5 Rno 40 4 1I 10 2,75 (I-5)

Insectivora

Cru 35 10 847 28,57 84,7 (1-800) Csu 4 3 7 75 2,33 (I-5) Eeu 5 Nan 2 2 115 100 57,50 (7-108) Sar 7 4 143 57,14 35,75 (23-59) Toc 18 7 33 38,88 4,7 (2-14)

Chiroptera

Ese I Rfe 7 Rhi 2 Ppi 3

Total 620 160 3955 25,80

Table 1.- Prevalence and intensity of parasitation of each of the hosts species captured. Asy=Apodemus sylvaticus; Cru = Crocidura russula; Csu «Crocidura suaveolens; Eeu =Erinaceus europaeus; Ese=Eptesicus serotinus; Mag=Microtus agrestis; Mdo=Mus domesticus; Nan = Neomys anomalus; Ppi =Pipistrellus pipistrellus; Rfe=Rhinolophus jerrumequinum; Rhi = Rhinolophus hipposideros; Rno = Rail us norvegicus; Rra=Rattus rattus; Sar=Sorex araneus; Toc=Talpa occidentalis. Glycyphagid mites in small mammals 119

Parasitized hosts

Species found Asy Mag Mdo Rra Rno

C.(M.) hypudaei 96 (27,04 0J0) (50 070) 9 (6,66 0J0) 3 (7,5 0J0) O. dispar I ( 0,28 0J0) O. soricis 7 ( 1,97 0J0) I (0,74 0J0) I (2,5 0J0) X. krameri 42 (11,86 0J0) 2 (1,48 0J0) Crammolichus sp. 14 ( 3,95 0J0) I (0,74 0J0)

Table 2.- Distribution of Glycyphagidae species on rodent hosts. ( ) = prevalence.

Parasitized hosts

Species found Cru Csu Eeu Nan Sar Toc

C.(M.) hypudaei 8 (22,85 0J0) I (25 0J0) I (14,29 0J0) I ( 5,55 0J0) L. talpae I ( 5,55 %) 0. dispar 6 (33,33 0J0) 0. soricis 3 ( 8,57 0J0) I (25 0J0) 2 (100 0J0) 4 (57,14 0J0) X. krameri 3 ( 8,57 0J0) 2 (50 0J0) I ( 5,55 0J0)

Table 3.- Distribution of Glycyphagidae species on insectivorous hosts. ( )= prevalence.

author to conclude (FAIN, 1968 b) that specimens tiformes). Revue de Zoologie et de Botanique Africaine, 78: previously identified as belonging to the genus 161-174. Lophuromyopus Fain, 1965 were in fact hypopial stages FAIN (A.), 1969 a.- Les deutonyrnphes hypopiales vivant en of the new genus. In the present study we have thus association phoretique sur les rnarnrniferes (Acarina: Sarcop- tiformes). Bulletin de l'lnstitut Royal des Sciences Naturelles de classified as Grammolichus sp. all hypo pi fitting the Belgique, 45: 1-262. descriptions previously published for Lophuromyopus. FAIN (A.), 1969 b.- Morphologie et cycle evolutif des Currently only 18 species of the genus Grammolichus are Glycyphagidae commensaux de la taupe (Talpa europaeai (Sar- known, and of these only one (G. eliomys Portus et Fain, coptiformes). Acarologia, 11: 750-795. 1982) has been cited in Spain, on Eliomys quercinus FAIN (A.) & LUKOSCHUS (F.S.), 1974.- Observations sur le ophiusae captured on the island of Formentera in the developpernent postembryonnaire des acariens de la famille Glycyphagidae a hypopes pilicoles ou endofoliculaires (Acarina: Balearics (PORTUS& FAI ,1982). These authors collected Astigmata). Bulletin de l'Academie Royale de Belgique (Sciences) and examined all the life cycle stages of the parasite, in- Serne serie, 60: 1137-1159. cluding adults, and were thus able to make a positive iden- GALLEGO (M.) & PORTUS (M.), 1982.- Sobre los acaros ec- tification. We found only hypopial stages of Gram- toparasitos de Insectivoros del Pirineo Catalan. In: III Reunion molichus sp. on 14 Apodemus sylvaticus and 1 Mus Anual de la Asociacion de Parasitologos Espaitoles (Madrid), domesticus. The absence of adults did not allow to iden- Abstracts of Papers, Madrid: 110. GALLEGO (M.) & PORTUS (M.), 1987.- Acaros parasites de los tify the species concerned. generos Mus y Apodemus en Cataluna. Revista Iberica de Parasitologia, Vo!. Extra.: 263-268. GALLEGO(M.), PORTUS(M.) & GALLEGO(1.), 1983.- Estudio corn- ACKNOWLEDGEME 1S parativo de la fauna acarina ectoparasitaria de Apodemus syivaticus Linnaeus, 1758 (Rodentia: Muridae) del Pirineo Oriental We would like to thank Prof. Or. A. Fain of the Institut Royal y de la Cordillera Costero-Catalana. In: !11 Congreso Nacional des Sciences Naturelles of Belgium for his invaluable assistance in de Parasitologia (Barcelona), Abstracts of Papers, Barcelona: 16. the identification of the glycyphagids reported in this study, and in GALLEGO (M.), PORTUS (M.) & GALLEGO (1.), 1988.- Acaros particular for his advice concerning the systematics and morphology parasites de micromamiferos en Cataluna. I: Familia of the genus Crammolichus. Glycyphagidae. Revista Iberica de Parasitologia, 48: 417-432. HAITLINGER (R.), 1977.- Parasitological investigation of small mammals of Gory Sowie. V. Acarina (Trombidiformes, Ixodides, REFERENCES Sarcoptiformes). Bulletin Entomologique de Pologne, 47: 377-427. LUKOSCHUS(F.S.), 1967.- Kratzmilben an spanischen Kleinsaugern FAIN (A.), 1968 a.- Acariens nidicoles et detricoles en Africa au (Psorergatidae: Trombidiformes). Revista Iberica de Parasitologia, Sud du Sahara. Ill. Especes et genres nouveaux dans les sous- 27: 201-221. families Labidophorinae et Grammolichinae (Glycyphagidae: Sar- PEREIRA-LoRE zo (A.), COUCE-CANEIRO (M.C.) & Q INTEIRO- coptiformes). Acarologia, 10: 86-110. ALONSO(M.P.), 1987.-Identificaci6n de ectoparasitos de Roden- FAIN (A.), 1968 b.- Acariens nidicoles et detricoles en Africa au tia e Insectivora capturados en Galicia. Ill. Orden Siphonaptera. Sud du Sahara. IV. Decouverte du cycle evolutif d'un Acarien du Revista Iberica de Parasitologia, Vol. Extra.: 251-254. genre Lophuromyopus Fain, 1965 (Glycyphagidae: Sarcop- PORTUS (M.) & FAI (A.), 1982.- Grammolichus eliomys 120 A. PEREIRA & J. CASTRO

(Glycyphagidae), a new mite with endofollicular hypo pi in the PORTUS(M.), ESPONERA(D.) & GALLEGO (M.), 1987.- Aportaci6n tail of the dormouse Eliomys quercinus ophiusae Thomas (Ro- al conocimiento de la biologia de los acaros ectoparasitos de la dentia, Gliridae) in Formentera Island, Spain. Acarologia, 23: Sierra de Collcerola (Barcelona). Ciclo anua!. Revista Iberica de 265-272. Parasitologia, Vo!. Extra.: 269-272.