Intestinal helminths infection of rats (Ratus norvegicus) in the Belgrade area (Serbia): the effect of sex, age and habitat

SUMMARY: Gastrointestinal helminths of Norway rat (Rattus norvegicus) from the Belgrade area were studied as a part of a wider ecological research of rats in Serbia (data on the distribution, population ecology, economic and epizoothiological-epidemiological importance, and density control). Rats were captured from May 2005 to July 2009 at both urban and suburban-rural sites. Of a total of 302 trapped rats 48% were males and 52% females, with 36.5% and 38.8% of juvenile-subadult individuals, per sex respectively. Intestinal helminth infection was noted in 68.5% of rats, with a higher prevalence in male hosts and in adult individuals. Higher numbers of infected juveniles-subadults were noted in suburban-rural habitats, while an opposite tendency was noted in adult rats. Seven helminth species were recovered, of which five were nematode (Heterakis spumosa, Nippostrongylus brasiliensis, Capillaria sp., Trichuris muns and Syphacia muris) and two cestode species (Hymenolepis diminuta and Rodentolepis fraterna). The most prevalent parasites were Heterakis spumosa (36.7%) and Hymenolepis diminuta (30.5 %). Sex and habitat-related differences were noted in the prevalence of infection with Capillaria sp. and Trichuris muris, while there were no age-related differences in the prevalence of infection with any individual helminth species. Significantly higher prevalence of infection was noted in summer as compared to spring or winter, with a tendency to be higher in autumn as compared to spring. The only significant difference in the prevalence of infection between habitat-related was noted during spring. H. spumosa was most prevalent in summer, while H. diminuta and N. brasiliensis in autumn. The mean intensity of infection with H. spumosa, R. fraterna, S. muris and T muris was higher in autumn than in the other seasons, while N. brasiliensis and Capillaria sp. occured in winter. No more than four helminth species were found in one host.     

Helminths from introduced small mammals on Kerguelen, Crozet, and Amsterdam Islands (southern Indian Ocean).

Four monoxenous nematodes and 1 heteroxenous cestode were found in 4 species of introduced small mammals on isolated sub-Antarctic islands of the Indian Ocean. In the Kerguelen Archipelago, Syphacia obvelata, Passalurus ambiguus (Nematoda: Oxyuridae), and Rodentolepis straminea (Cestoda: Cyclophyllidae) were respectively found in the house mouse Mus musculus, the rabbit Oryctolagus cuniculus, and the black rat Rattus rattus. One accidental nematode, Trichostrongylus sp. (Nematoda: Trichostrongylidae), was also found in a black rat on Kerguelen. On Possession Island (Crozet Archipelago), R. straminea was present in the black rat. On Amsterdam Island, the brown rat R. norvegicus harbored 2 species, R. straminea and Nippostrongylus brasiliensis (Nematoda: Heligmonellidae). The small number of founder hosts and the depauperate terrestrial communities on these remote islands explain the low diversity in the helminth communities of these introduced mammals compared with continental populations.     

Detection of Streptobacillus spp. in feral rats by specific polymerase chain reaction

Streptobacillus moniliformis is an etiological agent of rat-bite fever and Haverhill fever in human infection. As the currently available methods for identifying the causative bacteria are not satisfactory, we attempted to establish them by PCR using newly designed primers for the 16S rRNA gene of S. moniliformis. We then determined the prevalence of Streptobacillus spp. in two species of feral rats that inhabit an urban region in Japan, because information on the prevalence of the bacteria in feral rats is obscure. The use of PCR with newly designed primers showed that an extremely high proportion of R. norvegicus harbored the bacteria (61/66, 92%), whereas the prevalence was only 58% in R. rattus (30/52). The nucleotide sequence analysis of the 16S rRNA gene of Streptobacillus spp. isolated from oral swabs of feral rats showed at least two different types of bacteria among isolates from R. norvegicus and R. rattus.     

Dating of divergences within the Rattus genus phylogeny using whole mitochondrial genomes

The timing and order of divergences within the genus Rattus have, to date, been quite speculative. In order to address these important issues we sequenced six new whole mitochondrial genomes from wild-caught specimens from four species, Rattus exulans, Rattus praetor, Rattus rattus and Rattus tanezumi. The only rat whole mitochondrial genomes available previously were all from Rattus norvegicus specimens. Our phylogenetic and dating analyses place the deepest divergence within Rattus at approximately 3.5 million years ago (Mya). This divergence separates the New Guinean endemic R. praetor lineage from the Asian lineages. Within the Asian/Island Southeast Asian clade R. norvegicus diverged earliest at approximately 2.9Mya. R. exulans and the ancestor of the sister species R. rattus and R. tanezumi subsequently diverged at approximately 2.2Mya, with R. rattus and R. tanezumi separating as recently as approximately 0.4Mya. Our results give both a better resolved species divergence order and diversification dates within Rattus than previous studies.     

Ag-NOR chromosomal association patterns in Rattus rattus (Rafinesque, 1814) and Rattus norvegicus (Berkenhout, 1796) from the southern Iberian peninsula

A high frequency of satellite association phenomena in a number of specimens of Rattus rattus and R. norvegicus, captured on the coastal fringe of Málaga province (Southern Spain), was found. Only Ag-NOR bearing chromosomes participated in associations in both species. R. rattus is characterized by 14/18 heterologous and R. norvegicus by 5/5 and 13/13 homologous association types.     

Epizootiological and epidemiological study of hantavirus infection in Japan

Epizootiological surveys on hantavirus infections in rodents were carried out in various areas of Japan, including the four major islands of Hokkaido, Honshu, Shikoku, and Kyushu from 2000 to 2003. A total of 1,221 rodents and insectivores were captured. Seropositive animals were found in Apodemus (A.) speciosus (5/482, 1.0%), Rattus (R.) norvegicus (4/364, 1.1%), R. rattus (3/45, 6.7%), and Clethrionomys (C.) rufocanus (7/197, 3.6%). The partial S segment was amplified from one seropositive R. rattus captured at Hakodate. The nucleotide sequence showed 96% identity with the Seoul virus (SEOV) prototype strain SR-11. In addition, we conducted an epidemiological survey on human hantavirus infection in a high-risk population, the personnel of the Japan Ground Self-defense Force on Hokkaido. One out of 207 human blood samples was positive for anti-hantavirus antibody by IFA, ELISA, and WB analysis. The result of the serotype specific ELISA indicates that this individual acquired SEOV infection. This study indicates that A. speciosus, R. norvegicus, R. rattus, and C. rufocanus carry hantaviruses as the reservoir animals in Japan. Infected R. rattus and R. norvegicus in port areas could be the sources of human SEOV infection and a threat to travelers and individuals working in seaports.     

A mathematical epidemiological model of gram-negative Bartonella bacteria: does differential ectoparasite load fully explain the differences in infection prevalence of Rattus rattus and Rattus norvegicus?

We postulate that the large difference in infection prevalence, 24% versus 5%, in R. norvegicus and R. rattus, respectively, between these two co-occurring host species may be due to differences in ectoparasite and potential vector infestation rates. A compartmental model, representative of an infectious system containing these two Rattus species and two ectoparasite vectors, was constructed and the coefficients of the forces of infection determined mathematically. The maximum difference obtained by the model in the prevalence of Bartonella in the two Rattus species amounts to 4.6%, compared to the observed mean difference of 19%. Results suggest the observed higher Bartonella infection prevalence in Rattus norvegicus compared to Rattus rattus, cannot be explained solely by higher ectoparasite load. The model also highlights the need for more detailed biological research on Bartonella infections in Rattus and the importance of the flea vector in the spread of this disease.     

Parasites in social subterranean Zambian mole-rats (Cryptomys spp., Bathyergidae, Rodentia)

Three out of 18 examined common mole-rats ( Cryptomys sp., Xkaryotype 2n = 58) from Zambia were infested with cestodes ( Inermicapsifer nmdagascariensis and an undetermined species) and a nematode ( Protospirura muricola ). Four out of 14 examined Zambian giant mole-rats ( Cryptomys mechowi ) hosted cestodes ( Raillietina (R) sp. and an undetermined species) and nematodes ( Protospirura muricola, Capillaria sp.). Helminths and circumstances of findings are briefly described. No ectoparasites were found. The influences of subterranean and social way of life and feeding habits upon occurrence of parasites in mole-rats are discussed. Burrow conditions and social behaviour seem not to favour infestation by parasites.     

The independent evolution of two closely related satellite DNA elements in rats (Rattus).

We have identified and determined the sequence and organization of a new rat satellite DNA in Rattus rattus, the roof rat. This satellite DNA, which we call R. rattus satellite I', consists of tandem arrays of a 185 base pair (bp) repeat unit that we call a'. a' is 86% homologous to a 185 bp portion of the 370 bp repeat unit of the previously described rat satellite [Pech et al. (1979) Nucleic Acids Res. 7, 417-432] present in the common laboratory rat species, R. norvegicus. We can thereby distinguish two 185 bp portions of the satellite I 370 bp repeat unit: "a" (homologous to a') and "b". Satellite I has the structure (a,b)n, and satellite I' has the structure (a')n. Like a, a' is only about 60% homologous to b and fails to hybridize to b. Although R. norvegicus and R. rattus contain about the same total concentration of satellite sequences, R. norvegicus contains essentially only the a,b type (satellite I), whereas R. rattus contains a' type (satellite I') and lesser amounts of the a,b type (satellite I). The a,b type (satellite I) in R. rattus is very similar to that in R. norvegicus as judged both by hybridization and by the presence of all but one of the major restriction enzyme sites that characterize the R. norvegicus satellite I. In R. rattus the a' and a,b repeat units are not detectably present in the same tandem array. All of the sequence differences between a' (R. rattus) and a (R. norvegicus) can be accounted for by simple base substitutions, and the implication of this and other features of rat satellite DNA structure for satellite DNA evolution are discussed.     

Isolation and characterization of microsatellites in Rattus rattus

We isolated and characterized 10 microsatellite loci in the black rat Rattus rattus (Muridae, Rodentia), a widespread invasive species largely known to cause serious problems in agriculture and human health. Polymorphism was studied in two populations, one from Madagascar and one from Senegal. It ranged from three to 12 alleles in Madagascar, and from two to five alleles in Senegal. Together with the loci previously adapted from Rattus norvegicus, this set of markers should allow the conduct of thorough studies on the genetic structure of natural populations of R. rattus.     

Parasitic helminths from Sigmodon hispidus (Rodentia: Cricetidae) from seasonal and evergreen habitats in Costa Rica

The helminthological fauna of the cotton rat, Sigmodon hispidus in a tropical environment varies according to habitat and feeding behavior. Six species of nematodes (Longistriata adunca, Trichostrongylus sigmodontis, Strongyloides sigmodontis, Litomosoides carinii, Monodontus sp. and Protospirura sp.) and two species of cestodes (Hymenolepis diminuta and Raillietina sp.) were found in rats from extensive dry lands in Guanacaste where hot temperatures and heterogeneous diet are the rule. Only two species of nematodes (Longistriata adunca and Angiostrongylus costaricensis) were found in rats collected in a humid pineapple plantation in the Central Plateau (Alajuela) where mild temperatures predominate. A. costaricensis, a metastrongylid of medical importance, was found in 42% of them.     

Seasonal studies on commensal rats and their ectoparasites in a rural area of Egypt: the relationship of ectoparasites to the species, locality, and relative abundance of the host.

The present study was carried out in 3 villages, namely Kafr Ayoub Soliman, Kafr Ibrahim El-Aidi, and El-Sa'adat, Sharqiya Governorate, Egypt. A total of 519 rats was collected from the 3 study sites: 46.6% Rattus rattus, and 53.4% Rattus norvegicus. A total of 20,643 ectoparasites was recovered from R. rattus: 33.3% mites, 33.8% fleas, and 32.9% lice. From R. norvegicus a total of 40,997 ectoparasites was recovered: 28.9% mites, 31% fleas, and 40.1% lice. Three common mite species were recovered from both rat hosts, i.e., Ornithonyssus bacoti, Radfordia ensifera, and Laelaps nuttalli. Three common flea species were also recovered from both rat hosts, i.e., Echidnophaga gallinacea, Leptopsylla segnis, and Xenopsylla cheopis. Polyplax spinulosa was the only dominant louse species that infested both rat hosts. Rats did not show a definite breeding season, and the seasonal rat indices were generally low in different study sites. There were no significant differences between the prevalence of each of mites, fleas, and lice in both rat species. The total general indices of mites and fleas, on the other hand, was significantly higher in R. norvegicus. The general index of X. cheopis was high and ranged between 5.9 in R. rattus and 14.5 in R. norvegicus. Season-related changes were observed in the general index of each of L. segnis infesting both rat species and R. ensifera and O. bacoti infesting R. norvegicus. The prevalence and general indices of some ectoparasites showed differences related to the locality of their rat hosts. Seasonal changes in the general indices of some ectoparasites paralleled seasonal changes in the relative abundance of their rat hosts.     

Parasitic zoonoses in Papua New Guinea

Relatively few species of zoonotic parasites have been recorded in humans in Papua New Guinea. A greater number of potentially zoonotic species, mostly nematodes, occur in animals but are yet to be reported from humans. Protozoa is the best represented group of those infecting man, with Giardia duodenalis, Cryptosporidium parvum, Cyclospora cayetanesis, Toxoplasma gondii, Sarcocystis spp., Entamoeba polecki, Balantidium coli and, possibly, Blastocystis hominis. The only zoonotic helminths infecting humans include the trematode Paragonimus westermani, the cestodes Hymenolepis nana, H. diminuta and the sparganum larva of Spirometra erinacea, and the nematodes Trichinella papuae and Angiostrongylus cantonensis and, possibly, Ascaris suum. Other groups represented are Acanthocephala (Macracanthorhynchus hirudinaceus)), insects (Chrysomya bezziana, Cimex sp., Ctenocephalides spp.), and mites (Leptotrombidium spp. and, possibly Sarcoptes scabiei, and Demodex sp.). One leech (Phytobdella lineata) may also be considered as being zoonotic. The paucity of zoonotic parasite species can be attributed to long historical isolation of the island of New Guinea and its people, and the absence until recent times of large placental mammals other than pig and dog. Some zoonotic helminths have entered the country with recent importation of domestic animals, in spite of quarantine regulations, and a few more (two cestodes, one nematode and one tick) are poised to enter from neighbouring countries, given the opportunity. Improvement in water supplies, human hygiene and sanitation would reduce the prevalence of many of these parasites, and thorough cooking of meat would lessen the risk of infection by some others.     

Gastrointestinal helminths of the northern bobwhite in Florida: 1968 and 1983

We collected 153 northern bobwhites (Colinus virginianus) over a 10-mo period from Tall Timbers Research Station near Tallahassee, Florida, USA. Five species of gastrointestinal helminths were encountered commonly (greater than 30% prevalence): Cyrnea colini, Raillietina cesticillus, R. colinia, Heterakis isolonche, and Trichostrongylus tenuis. Other helminths included Brachylaima sp., Rhabdometra odiosa, Mediorhynchus papillosis, Cheilospirura spinosa, Dispharynx nasuta, Gongylonema ingluvicola, and Tetrameres pattersoni. During the intervening 15 yr since the last year-round study of this population of birds, C. spinosa and T. pattersoni have declined markedly, and Strongyloides sp. probably has become extinct locally. Prevalence and intensity seem more likely to fluctuate in parasite species that have complex life cycles.     

Habitat associations of small mammals in southern Brazil and use of regurgitated pellets of birds of prey for inventorying a local fauna.

We inventoried terrestrial small mammals in an agricultural area in southern Brazil by using trapping and prey consumed by Barn Owls (Tyto alba) and White-tailed Kites (Elanus leucurus). Small mammals were trapped in three habitat types: corn fields, uncultivated fields ("capoeiras"), and native forest fragments. A total of 1,975 small mammal specimens were trapped, another 2,062 identified from the diet of Barn Owls, and 2,066 from the diet of White-tailed Kites. Both trapping and prey in the predators' diet yielded 18 small mammal species: three marsupials (Didelphis albiventris, Gracilinanus agilis, and Monodelphis dimidiata) and 15 rodents (Akodon paranaensis, Bruceppatersonius iheringi, Calomys sp., Cavia aperea, Euryzygomatomys spinosus, Holochilus brasiliensis, Mus musculus, Necromys lasiurus, Nectomys squamipes, Oligoryzomys nigripes, Oryzomys angouya, Oxymycterus sp.1, Oxymycterus sp.2, Rattus norvegicus, and Rattus rattus (Linnaeus, 1758)). The greatest richness was found in the uncultivated habitat. We concluded that the three methods studied for inventorying small mammals (prey in the diet of Barn Owls, White-tailed Kites, and trapping) were complementary, since together, rather than separately, they produced a better picture of local richness.     

Influence of habitat modification on the community of gastrointestinal helminths of cotton rats.

Dynamics of communities of gastrointestinal helminths of cotton rats (Sigmodon hispidus) were monitored in response to five experimental brush management treatments using herbicide applications with and without prescribed burning on the Cross Timbers Experimental Range in Payne County, Oklahoma (USA). A total of 113 adult cotton rats (68 male and 45 female) was collected from experimental pastures in winter and summer 1986 resulting in the recovery of five species of helminths: Longistriata adunca, Syphacia sigmodontis, Strongyloides sp., Protospirura muris, and Raillietina sp. Prevalences of Raillietina sp. and S. sigmodontis were greater on control than herbicide-treated pastures. Prevalence and abundance of Raillietina sp. and prevalence of S. sigmodontis were significantly lower on annually burned, herbicide-treated pastures compared to unburned herbicide-treated pastures. Triclopyr-treated pastures had greater abundances of L. adunca and lower abundances of Raillietina sp. than those treated with tebuthiuron. Abundances of L. adunca also decreased from winter to summer on annually burned, herbicide-treated pastures while increasing on other pastures. Distribution of all helminths was overdispersed, but distribution of L. adunca showed a significant brush treatment by season interaction as a result of greater overdispersion in summer than winter for cotton rats inhabiting brush-treated pastures. Our results indicate that man-induced habitat modifications can alter host-parasite relationships in the community.     

The discovery of Besnoitia wallacei in Australia and the identification of a free-living intermediate host

A cat fed free-living rats (Rattus norvegicus and Rattus rattus) passed coccidian oocysts 14 days after eating a R. norvegicus. These oocysts were morphologically similar to B. wallacei and rats and mice dosed orally and intraperitoneally with them developed Besnoitia cysts in various body tissues. This organism was shown to have an obligatory two-host cycle and it is considered to be B. wallacei. This represents the first recorded detection of B. wallacei in Australia and also the first record of a natural free-living intermediate host for B. wallacei.     

Observations on commensal rats and their status to plague in Bombay

The distribution pattern of various types of commensal rodents in Bombay city reveals that Bandicota bengalensis constitutes the predominant commensal rodent species followed by R. rattus and Rattus norvegicus. Apart from these three types, Bandicota indica, M. musculus and an insectivore (Suncus murinus) are the three species of commensal small mammals that are frequently encountered in or near human habitations. These small mammals are prevalent throughout the year and their percentage distribution varies very little during different months of the year. None of the rodent species examined during the years 1976-85 revealed presence of Y. pestis infection by bacteriological or serological methods. From these findings, it could be concluded that in the city of Bombay a focus of zoonotic plague infection does not exist.     

Distribution and insecticide resistance of the plague flea Xenopsylla cheopis in Maharashtra State, India

Distributions are reported for commensal rat fleas, predominantly Xenopsylla cheopis (Rothschild), in the State of Maharashtra, India, including the city of Bombay, during 1965-80. The X.cheopis flea index was high in most parts of Maharashtra, but low in Bombay. Rattus rattus Linnaeus is the principal host of X.cheopis, but the host range includes Bandicota bengalensis Gray, Golunda ellioti Gray, Mus musculus Linnaeus, Rattus blandfordi Thomas, R. norvegicus Berkenhout, Suncus caerulaeus Lerr, S. murinus Linnaeus and Tatera indica Hardwicke. X.cheopis was found to have high degrees of resistance to DDT, malathion and fenthion, tolerance to gamma HCH (= gamma BCH) but susceptibility to dieldrin. This insecticide resistance situation may contribute to the high flea indices prevailing in the state, with consequent risks of plague outbreaks. Two other species of rat flea, X.astia Rothschild and X.brasiliensis (Baker) were found to be less common than previously recorded. Their apparent replacement by X.cheopis is tentatively attributed, at least partly, to the selective advantage of insecticide resistance in the latter species.