Helminth Fauna of Commensal Rodents, Mus musculus (Linnaeus, 1758) and Rattus rattus (Linnaeus, 1758) (Rodentia, Muridae) in Sicily (Italy)

Transcription

1 Artículo de Original Helminth Fauna of Commensal Rodents, Mus musculus (Linnaeus, 1758) and Rattus rattus (Linnaeus, 1758) (Rodentia, Muridae) in Sicily (Italy) MILAZZO C. 1, CAGNIN M. 1, DI BELLA C. 2, GERACI F 2 and RIBAS A. 3,4 1 Department of Ecology, University of Calabria, Via P. Bucci s/n, Arcavacata di Rende, Cosenza (Italy). 2 Area di Sorveglianza epidemiologica, Istituto Zooprofilattico Sperimentale della Sicilia, Via Marinuzzi Gino, 4, Palermo (Italy). 3 Laboratory of Parasitology, Faculty of Pharmacy, University of Barcelona, Avda Diagonal s/n Barcelona (Spain). 4 Institut de Recerca de la Biodiversitat, Facultat de Biologia, Universitat de Barcelona, Avda Diagonal Barcelona (Spain). ABSTRACT Seventy-three house mice (Mus musculus) and forty black rats (Rattus rattus) from Palermo (Sicily, Italy) were examined for the presence of helminth parasites. The study was carried out in 18 localities during the period March-December Mus musculus harbored one species of Digenea (Brachylaima sp.), one species of cestode (Taenia taeniaeformis larvae) and eight species of nematode (Syphacia obvelata, Aspiculuris tetraptera, Mastophorus muris, Heterakis spumosa, Trichuris muris, Capillaria hepatica, Heligmosomoides polygyrus and Nippostrongylus brasiliensis). Rattus rattus harbored one species of Digenea (Brachylaima sp.), two species of cestode (Hymenolepis diminuta, Rodentolepis nana), seven species of nematode (Syphacia muris, Aspiculuris tetraptera, Mastophorus muris, Heterakis spumosa, Capillaria hepatica, Eucoleus gastricus and Nippostrongylus brasiliensis) and one unidentified species of acanthocephalan. The overall prevalence of infection of the house mouse (M. musculus) was 61.64% and that of the black rat (R. rattus) was 92.68%. Key words: Acanthocephalan, cestode, helminth, Mus musculus, nematode, parasite, Rattus rattus, rodent, Sicily, trematode. RESUMEN Setenta y tres ratones domésticos (Mus musculus) y cuarenta ratas negras (Rattus rattus) procedentes de Palermo (Sicilia, Italia) fueron examinadas para para evidenciar la presencia de helmintos. El presente estudio se realizó en 18 localidades durante el periodo marzo-diciembre Mus musculus presentó una especie de Digenea (Brachylaima sp.), otra de Cestoda (Taenia taeniaeformis larvae) y ocho de Received: 10 September Accepted: 24 September Corresponding: Alexis Ribas Laboratory of Parasitology, Faculty of Pharmacy, University of Barcelona Avinguda Diagonal s/n Barcelona (Spain). aribas@ub.edu 194

2 HELMINTH OF COMMENSAL RODENTS IN SICILY (ITALY) Nematoda (Syphacia obvelata, Aspiculuris tetraptera, Mastophorus muris, Heterakis spumosa, Trichuris muris, Capillaria hepatica, Heligmosomoides polygyrus y Nippostrongylus brasiliensis). En Rattus rattus se halló una especie de Digenea (Brachylaima sp.), dos de cestodos (Hymenolepis diminuta, Rodentolepis nana), siete de nematodos (Syphacia muris, Aspiculuris tetraptera, Mastophorus muris, Heterakis spumosa, Capillaria hepatica, Eucoleus gastricus y Nippostrongylus brasiliensis) y otra no identificada de acantocéfalo. La prevalencia de parasitación fue del 61,64% y del 92,68% en M. musculus y en R. rattus, respectivamente. Palabras clave: Acantocéfalo, cestodo, helminto, Mus musculus, nematodo, parásito, Rattus rattus, roedor, Sicilia, trematodo. INTRODUCTION Researches on helminths in sympatric urban populations of Rattus rattus and Mus musculus are scarce, and they have been performed mainly in tropical areas (Rafique et al., 2009). To our knowledge, however, such works have not been conducted in Europe. Previous studies on both species are limited to wild populations (Feliu et al., 1985; Milazzo et al., 2003). Other studies, moreover, have examined a single species: urban M. musculus (Landaeta-Aqueveque et al., 2007; Kataranovsku et al., 2008) or R. rattus (Mafiana et al., 1997; Waugh et al., 2006). The present study attempts to fill this gap by analyzing helminths of both rodent species in sympatric urban populations in Sicily. MATERIAL AND METHODS The rodents examined in the present study were collected in 18 localities (gardens and lots) in the city of Palermo, Sicily Island (Italy). Rats (25 males and 16 females, 3 juveniles and 58 adults) and mice (37 males and 36 females, 15 juveniles and 58 adults) were trapped from March to December Rodents were captured using metallic live traps (Havahart or Longworth models). Mice were separated into two age-weight groups: juveniles (< 9 to < 12 g) and adults ( 12 to > 15 g) (Krebs et al., 1995). Rats were ranked by weight as juveniles (< 100 g) and adult (> 130 g) (Delattre and Le Louar, 1981). Stomach, intestine, liver, pancreas and lungs were separated and examined for helminths. The worms recovered were mounted permanently in Canada balsam or temporally examined in Amann lactophenol. Prevalence and mean intensity of the parasitic helminths were calculated following Bush et al. (1997). The Kruskal Wallis test was used to assess the difference in intensity for sex and host age (adult/juvenile). The difference in parasite prevalence was examined using Chi-square tests (χ 2 ). Statistical analyses were performed using the software SAS System 9.1 for Windows. Significance was assumed for P > RESULTS The helminth community consisted of fifteen parasitic species (Table 1). Voucher specimens of each species of parasite and from both host were deposited in Museu de Ciències Naturals de Barcelona (Barcelona Natural Science Museum, Catalonia, Spain), codes MZB to Individuals of Brachylaima sp. could not be identified to species (Ribas et al., 2005). The nematode C. hepatica, could not be counted because only eggs and damaged individuals were recovered from the liver, occurrence was assessed on the basis of the presence of eggs (Resendes at al., 2009). The overall prevalence of infection was 61.64% in the mice and 92.68% in the rats. The mean intensity of infection ± SD was ± in mice and ± in the rat. In M. musculus the predominant parasite species was the nematode S. obvelata, followed by the nematodes A. tetraptera and H. spumosa. In R. rattus, the most prevalent helminths were the nematodes M. muris (78.05%) and E. gastricus (65.85%), and the tapeworm H. diminuta (39.02%). No significant differences related to sex or age vs general prevalence or median intensity were found in either rodent. A single helminth species was isolated in 48.8% of the mice, two species 195

3 C. MILAZZO et al. Table 1. Helminths recovered from commensal rodents in Palermo, N = number of analysed hosts, P% = prevalence, MI = mean intensity, ± SD = standard deviation, RI = range of intensity Mus musculus (n = 73) Rattus rattus (n = 41) Helminth species P% MI ± SD RI P % MI ± SD RI TREMATODA Brachylaima sp CESTODA Hymenolepis diminuta Rodentolepis nana Taenia taeniaeformis (larvae) NEMATODA Aspiculuris tetraptera Capillaria hepatica Eucoleus gastricus Heligmosomoides polygyrus Heterakis spumosa Mastophorus muris Nippostrongylus brasiliensis Syphacia obvelata Syphacia muris Trichuris muris ACANTHOCEPHALA Acanthocephalan sp were found in 35.6% and three species were found in 15.6%. DISCUSSION The present study adds to our knowledge of helminths in urban rodents in Sicily, as previous reports dealt with wild rodents (Virga et al., 1995; Gouy de Bellocq et al., 2003; Milazzo et al., 2003). Among the helminth species reported for the house mouse, the cestode T. taeniaeformis and the nematodes H. polygyrus, H. spumosa and N. brasiliensis are new findings for this host in Sicily. In the black rat we report for the first time the presence of Brachylaima sp., A. tetraptera, E. gastricus, N. brasiliensis and acanthocephalans in Sicily. Our results show that species richness (twelve species) is higher for urban R. rattus than in the wild populations (five species) (Milazzo et al., 2003). In contrast, Mus musculus shows the same value in the present study (ten helminth species) as that reported in wild populations (Milazzo et al., 2003) (Table 2). The presence of Brachylaima sp., in which terrestrial snails act as first and second intermediate hosts, reveals the importance of gastropods in the diet of these two rodents in these urban areas. However, it is common in wild populations of both rodents (Feliu, 1985). The cestode H. diminuta was only recorded in R. rattus despite the considerable number of M. musculus that were examined. This is in accordance with previous studies; thus, in the compilation of Milazzo et al. (2003), this cestode was recorded from R. rattus in the seven Mediterranean islands analyzed, in contrast to the two islands on which it was found on M. musculus. Taenia taeniaeformis was not recorded from R. rattus; the definitive hosts are cats (Torres et al., 1989), which are infected mainly by mice. To our knowledge there are no studies on diet of feral cats in Palermo that might help us to establish whether their preference for mice rather than rats in urban conditions could explain these differences. The higher prevalence of this cestode in peridomestic M. musculus than in wild populations was previously noted by Feliu (1985). The nematode H. polygyrus is a specific parasite of rodent hosts of genus Apodemus, but extremely rare on the mainland in other hosts (Durette-Desset, 1968). The presence of H. poly- 196

4 HELMINTH OF COMMENSAL RODENTS IN SICILY (ITALY) Table 2. Helminth species recorded in Rattus rattus and Mus musculus in different habitats in Sicily Helminth species Mus musculus Mus musculus Rattus rattus Rattus rattus (n = 44) (n = 73) (n = 44) (n = 41) wild commensal wild commensal Milazzo et al. (2003) present study Milazzo et al. (2003) present study TREMATODA Brachylaima sp. * * * CESTODA Hymenolepis diminuta * * * Rodentolepis nana * Rodentolepis microstoma * Catenotaenia pusilla * Taenia taeniaeformis (larvae) * NEMATODA Aspiculuris tetraptera * * * Capillaria hepatica * * * * Eucoleus gastricus * Heligmosomoides polygyrus * Heterakis spumosa * * * Mastophorus muris * * * * Nippostrongylus brasiliensis * * Syphacia obvelata * * Syphacia muris * * Trichuris muris * * Gongylonema musculi * ACANTHOCEPHALA Acanthocephalan sp. * gyrus in Sicily can be attributed to the decrease in host specificity of helminth parasites in islands, as stated by Goüy de Bellocq et al. (2002). The enlargement of the ecological niche of H. polygyrus from Apodemus. sylvaticus (the wood mouse) to M. musculus was demonstrated, using genetic analysis in Corsica, by Nierbering et al. (2006). The presence of this nematode in M. musculus was only previously recorded in Corsica and Japan (Hasegawa, 1983). H. spumosa and N. brasiliensis are typical parasites of the genus Rattus (Feliu, 1980; Torres, 1988), being reported by Milazzo et al., (2003) in wild black rats in Sicily, while they did not find them in the wild house mouse. The presence of H. spumosa in M. musculus with a considerable prevalence (17.81%) suggests a greater ecological contact of the parasite with the black rat (prevalence 34.15%) than in rural habitats. A similar case was found in N. brasiliensis, which showed higher prevalence in R. rattus than in M. musculus, 9.51% and 6.85%, respectively (Table 1) although it is indeed a typical species of the genus Rattus (Feliu, 1980; Torres, 1988). S. obvelata and S. muris showed a clear specificity for each host in spite of the fact that they have the same location in the host (caecum), following a different pattern from H. spumosa (upper colon) and N. brasiliensis (small intestine). Future studies are required to increase our knowledge of the differences in helminth communities between rural and urban habitats in mice and rats, since most previous studies only deal with one species of rodent. REFERENCES 1. BUSH AO, LAFFERTY KD, LOTZ JM, SHOSTAK AW Parasitology meets ecology on its own 197

5 C. MILAZZO et al. terms: Margolis et al. revisited. J Parasitol 83: DELATTRE P, LE LOUAR H Dynamique des populations du rat noir (Rattus rattus) mangrove lacustre. Mammalia 45: DURETTE-DESSET MC Identification des strongles des mulots et campagnols dècrits per Dujardin. Ann Parasit Hum Comp 43: FELIU C, TORRES J, GALLEGO J, GOSÁLBEZ J, VENTURA J Primeros datos acerca de la helminthofauna de los Roedores del Delta del Ebro (Península Ibérica). Miscel Zool 9: GOÜY DE BELLOCQ J, MORAND S, FELIU C Patterns of parasite species richness of Western Palaeartic micromammals: island effects. Ecography 25: GOÜY DE BELLOCQ J, SARÀ M, CASANOVA JC, FELIU C, MORAND S A comparison of the structure of helminth communities in the woodmouse, Apodemus sylvaticus, on islands of the western Mediterranean and continental Europe. Parasitol Res: 90: HASEGAWA H, OTSURU M, TOBITA K Heligmosomoides polygyrus new record from Japan Nematoda, Heligmosomidae. Jap J Parasitol 32: KATARANOVSKU DS, OLIVERA D, VUKIĆEVIĆ- RADIĆ D, KATARANOVSKI MV, DUŠICA L, RADOVIĆ DL, MIRKOV II Helminth fauna of Mus musculus Linnaeus, 1758 from the suburban area of Belgrade, Serbia. Arc Biol Sci 60: LANDAETA-AQUEVEQUE CA, ROBLES MDR, CALLAN PE The community of gastrointestinal helminths in the housemouse, Mus musculus, in Santiago, Chile. Parasitol latinoam 62: MAFIANA CF, OSHO MB, SAM-WOBO S Gastrointestinal helminth parasites of the black rat (Rattus rattus) in Abeokuta, southwest Nigeria. J Helminthol 71: MILAZZO C, GOÜY DE BELLOCQ J, CAGNIN M, CASANOVA JC, DI BELLA C, FELIU C, MORAND S, SANTALLA F Helminths and ectoparasites of Rattus rattus and Mus domesticus from Sicily. Comp Parasitol 70: KREBS CJ, KENNEY AJ, SINGLETON GR Movements of feral house mice in agricultural landscapes. Austral J Zool 43: NIEBERDING C, MORAND S, LIBOIS R, MICH- AUX J Parasites and the island syndrome: the colonization of the western Mediterranean islands by Heligmosomoides polygyrus (Dujardin, 1845). J Biogeogr 33: RAFIQUE A, RANA SA, KHAN HA, SOHAIL A Prevalence of some helminthes in rodents captured from different city structures including poultry farms and human population of Faisalabad, Pakistan. Pak Vet J 29: RESENDES AR, AMARAL AFS, RODRIGUES A, ALMERIA S Prevalence of Calodium hepaticum (Syn. Capillaria hepatica) in house mice (Mus musculus) in the Azores archipelago. Vet Parasit 160: RIBAS A, CASANOVA JC, MIQUEL J, FONS R, GUISSET C, FELIU C On the fauna of digenetic trematodes, parasites of small mammals in the Natural Reserves of Py and Mantet (Oriental Pyrenees, France). Helminthologia 42: TORRES J, CASANOVA JC, FELIU C, GISBERT J, MANFREDI MT Contribución al conocimiento de la cestodofauna de Felis silvestris Schreber 1777 (Carnívora: Felidae) en la P. Ibérica. Rev Ibér Parasitol 49: VIRGA A, CANESTRI TROTTI G, NOBILE L, PAM- PIGLIONE S Elminti intestinali di roditori selvatici della Sicilia Occidentale. Atti Soc Ital Sci Vet 49: WAUGH CA, LINDO JF, FORONDA P, ÁNGELES- SANTANA M, LORENZO-MORALES J, ROBIN- SON RD Population distribution and zoonotic potential of gastrointestinal helminths of wild rats Rattus rattus and R. norvegicus from Jamaica. J Parasitol 42: Acknowledgments: This study was supported by the 60% program of Italian MIUR, University of Calabria (local coordinator M. Cagnin) and by a project of the Istituto Zooprofilattico della Sicilia (IZS SI 008/00) (local coordinator C. Di Bella). We want to thank G. Aloise for the help in the trapping. A. Ribas was supported by 2009-SGR-403 of the Government of Catalonia (Spain). We thank the two anonymous referees for their valuable comments to the manuscript and their constructive suggestions. 198