The aims of this research were: 1) to determine the helminth parasite fauna of seventy two Rattus norvegicus (Berkenhout, 1769) individuals inhabiting poultry farms in the Pampean region of Argentina; 2) to examine the relationship between parasitism and individual characteristics of the hosts, and 3) to analyze the associations among helminths. The study was carried out in twenty-four poultry farms from autumn 2000 to winter 2001. Nematodes were found in the intestine or caecum rectum of the 74 % of rats and cestodes were found along all the intestine of the 28 % of rats. Heterakis spumosa (Travassos 1914) was a central species, whereas Syphacia muris, Yamaguti 1941, Nippostrongylus brasiliensis (Travassos 1914) and Hymenolepis diminuta (Rudolphi 1819) were satellite species. Helminths do not affect rat survival and growth of rats. Rats parasitized with H. spumosa and H. diminuta were larger and older than non-parasitized rats. The intensity of infection with H. spumosa significantly increased with rat age. Rats parasitized with Nippostrongylus brasiliensis and Syphacia muris did not differ in size and age with respect to non-parasitized ones. The mean intensity of infections per host was 33.74, 74.28, higher than 200, and 3.10 for H. spumosa, S. muris, N. brasiliensis and H. diminuta, respectively. The mean intensity of infection with H. spumosa was higher in summer than in the other seasons, while the higher mean intensity of infection with N. brasiliensis and S. muris occurred in autumn. Infections with Heterakis spumosa and Syphacia muris, and with Syphacia muris and Nippostrongylus brasiliensis were independent; while Heterakis spumosa and Nippostrongylus brasiliensis were negatively associated.Centro de Estudios Parasitológicos y de VectoresFacultad de Ciencias Naturales y Muse

Busch, M.

Gomez Villafañe, Isabel Elisa

Robles, María del Rosario

Helminthologia

English

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©2008 Parasitological Institute of SAS, Košice  
DOI 10.2478/s11687-008-0024-1 
 
 
126 
 
 
 
Summary 
 
The aims of this research were: 1) to determine the 
helminth parasite fauna of seventy two Rattus norvegicus 
(Berkenhout, 1769) individuals  inhabiting poultry farms in 
the Pampean region of Argentina; 2) to examine the rela-
tionship between parasitism and individual characteristics 
of the hosts, and 3) to analyze the associations among 
helminths. The study was carried out in twenty-four poul-
try farms from autumn 2000 to winter 2001. Nematodes 
were found in the intestine or caecum rectum of the 74 % 
of rats and cestodes were found along all the intestine of 
the 28 % of rats. Heterakis spumosa (Travassos 1914) was 
a central species, whereas Syphacia muris, Yamaguti 1941, 
Nippostrongylus brasiliensis (Travassos 1914) and Hy-
menolepis diminuta (Rudolphi 1819) were satellite species. 
Helminths do not affect rat survival and growth of rats. 
Rats parasitized with H. spumosa and H. diminuta were 
larger and older than non-parasitized rats. The intensity of 
infection with H. spumosa significantly increased with rat 
age. Rats parasitized with Nippostrongylus brasiliensis and 
Syphacia muris did not differ in size and age with respect 
to non-parasitized ones. The mean intensity of infections 
per host was 33.74, 74.28, higher than 200, and 3.10 for H. 
spumosa, S. muris, N. brasiliensis and H. diminuta, respec-
tively. The mean intensity of infection with H. spumosa 
was higher in summer than in the other seasons, while the 
higher mean intensity of infection with N. brasiliensis and 
S. muris occurred in autumn. Infections with Heterakis 
spumosa and Syphacia muris, and with Syphacia muris and 
Nippostrongylus brasiliensis were independent; while 
Heterakis spumosa and Nippostrongylus brasiliensis were 
negatively associated. 
 
Key words: helminths; Heterakis spumosa; Hymenolepis 
diminuta; Nippostrongylus brasiliensis; Rattus norvegicus; 
Syphacia muris 
 
 
Introduction 
  
Parasitic infections are one of the factors that influences 
population dynamics, not only directly by affecting repro-
ductive or survival parameters of one species, but also 
indirectly by changing both intra and interspecific interac-
tions, decreasing competitive abilities or increasing vul-
nerability to predators. Although parasites rarely kill their 
hosts, they can produce a reduction in body mass, size 
and/or a change in behavior that ultimately may affect 
reproduction or survival of them. To evaluate the role of 
parasitism on the population dynamics of a species, is 
necessary to study both populations, the host and the para-
site (Wisnivesky, 2003). 
Helminth species such as Hymenolepis diminuta (Rudolphi 
1819); Taenia taeniaeformis (Batsch 1786); Capillaria 
hepatica (Bancroft 1893); Syphacia muris Yamaguti 1941; 
Nippostrongylus brasiliensis (Travassos 1914); Heterakis 
spumosa Schneider, 1866 and Toxocara spp. are associated 
to Rattus norvegicus (Berkenhout, 1769). These helminths 
have been cited in numerous studies, but these consist of 
descriptions, lists and new records of hosts and localities, 
and do not provide data about the relationship between the 
helminths and the individual characteristics of their hosts 
(Seong et al., 1995; Cabrera & Mendoza, 2001; Pinto et 
al.; 2001; Iannacone & Alvariño, 2002, Stojcevic et al., 
2004). However, the presence and the intensity of the para-
sites are related with the characteristics of the host, the 
interaction among the parasites (intraspecific and inter-
specific competition), and with the external environment 
(Iannacone & Alvariño, 2002; Stojcevic et al., 2004). On 
other hand,  of  the surveys that were carried out of ro-
dents, there have been only limited reports on intestinal 
parasites of rats (Suriano & Navone, 1992, 1994; Seong et 
al., 1995; Cabrera & Mendoza, 2001; Pinto et al., 2001; 
Iannacone & Alvariño, 2002).  
The aims of this work were: 1) to determine the helminth 
parasite fauna of R. norvegicus individuals that inhabiting 
poultry farms in the Pampean region of Argentina; 2) to 
HELMINTHOLOGIA, 45, 3: 126 – 129, 2008 
 
 
Helminth communities and host- parasite relationships  
in argentine brown rat (Rattus norvegicus) 
 
 
I. E. GOMEZ VILLAFAÑE1,2, M. R. ROBLES2,3, M. BUSCH1,2 
 
 
1Laboratorio de Ecología de Poblaciones. Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, 
Buenos Aires, Argentina, E-mail: isabelgv@ege.fcen.uba.ar; 2Consejo Nacional de Investigaciones Científicas y 
Tecnicas, Buenos Aires, Argentina; 3Centro de Estudios Parasitológicos y de Vectores CEPAVE (CCT- CONICET- 
La Plata) (UNLP), Calle 2 N° 584, 1900 La Plata, Buenos Aires, Argentina 
 
 
 
 
 
 
127
examine the relationship between parasitism and individual 
characteristics of the hosts, and 3) to analyze the associa-
tions among helminths.  
 
Materials and methods 
 
The study was carried out in Exaltación de la Cruz, Buenos 
Aires Province, Argentina, 34° S, 59° W. The study area is 
located in the Pampa Ondulada and has a temperate cli-
mate. Mean annual temperature is 16 °C, and annual rain-
fall averages 1000 mm. Rat samplings were conducted 
from autumn 2000 to winter 2001 in twenty-four poultry 
farms random selected among fifty-five poultry farms of 
the study area. Rats were captured in live traps of 15 x 16 x 
31 cm. Traps were baited with meat and carrot, and were 
active for three consecutive nights per farm and season. 
We studied six farms per season of each year. For each rat 
captured we recorded species according with external and 
cranial morphology, body mass (in g), size (in cm) and age 
(months). The age was estimated on based of the dry 
weight of the eye lens (Kataranovski et al., 1994). All 
individuals were manipulated according with the norms of 
the National law N° 14.346 of Argentina. 
We examined three portions of equal length of the intestine 
(upper intestine, medium intestine and lower intestine), and 
the caecum-rectum for the presence of helminths. 
Helminths were fixed in alcohol 70°, cleared with lacto-
phenol and observed under a microscope. The cestodes 
collected were stained in acetic carmin, dehydrated in a 
series of alcohols and mounted in Canada balsam. For the 
identification to the generic level we used the taxonomic 
key of Khalil et al. (1994) and Anderson et al. (1974). 
Voucher specimens were deposited in the Helminthologi-
cal Collection of Museo de La Plata (H. spumosa 5579, S. 
muris 5580, N. brasiliensis 5872, H. diminuta 5871), and 
their host, R. norvegicus, were deposited in the Mammals 
collection of Museo de La Plata (MLP 1.I.03.11, MLP 
1.I.03.12, MLP 1.I.03.13), La Plata, Buenos Aires Provin-
ce, Argentina. 
Prevalence and mean intensity of the helminths were cal-
culated following Bush et al. (1997). For the nematode N. 
brasiliensis and for the cestode H. diminuta we calculated 
the minimum intensity because of the difficulty in sepa-
rating the individual parasites in the first case and the diffi-
culty to extracting the whole parasites in the second case. 
We classified parasite species on basis of to their preva-
lence as: central if it was present in more than 2/3 of the 
hosts, secondary if it was present between 1/3 and 2/3 of 
the hosts and satellite, if it was present in less than 1/3 of 
the hosts (Bush & Holmes, 1986).  
We compared the body mass and age of parasitized and 
non- parasitized hosts by means of T- test of independent 
samples or U-Mann Whitney test depending if the data 
fulfilled the assumptions of normality and covariance (Zar, 
1996). To evaluate if the intensity of infection increases 
along the life of hosts, we studied the association between 
the mean intensity and the age of individuals by means of a 
Spearman correlation (Zar, 1996). We compared the inten-
sity of infection among seasons by means of a Kruskall-
Wallis test (Zar, 1996).  
We studied the existence of associations between the in-
fections with different nematode species analyzing the 
frequency of co-occurrence of two species in the same 
individual by means of Chi-square test (Yates’ correction) 
(Zar, 1996) and Forbes Index (Dice 1945) for determining 
if the frequency of coexistence was lower (Forbes<1) or 
higher than expected (Forbes>1) by chance.  
 
Results 
 
A total of 72 R. norvegicus were captured during the study 
period. Nematodes were found in the intestine or caecum 
rectum of the 74 % of rats, and cestodes were found along 
all the intestine of the 28 % of rats. Nematodes include H. 
spumosa; S. muris and N. brasiliensis; whereas only one 
species of the cestode, H. diminuta, was found. 
H. spumosa was a central species with a prevalence of 66 %, 
whereas H. diminuta, S. muris and N. brasiliensis were 
satellite species, with a prevalence of 28 %, 14 % and 11 % 
respectively. There were two rats infected with three species 
of nematodes simultaneously. 
H. spumosa was localized in the lower intestine and/or 
caecum-rectum. Body mass and age of rats parasitized (P) 
with H. spumosa were significantly higher than those of 
not parasitized (NP) (BODY MASS: meanP=301 g; SdP = 
94.7 and meanNP = 212 g; SdNP = 112.1; respectively; t74 = 
3.71; p < 0.001; AGE: medianP = 6 months; Q1 = 3.9; Q3 = 
7.1 and medianNP = 4 months, Q1 = 1.8; Q3 = 5.8, respec-
tively; U73 = 463; p = 0.02; Fig. 1a). There was a signifi-
cant positive association between intensity of infection 
(mean intensity= 33.74; Sd = 53.15) with H. spumosa and 
the age of rats (rs = 0.34; p < 0.05). Mean intensity varied 
among seasons (H7,40 = 14.56; p = 0.012), being greater in 
Summer than Autumn 2000 (H1,28 = 4.81; p = 0.028) and 
Winter 2001 (H1,18; p = 0.001), and marginally greater than 
Spring (H1,18 = 3.30; p = 0.069). 
Nippostrongylus brasiliensis was localized in the  upper 
intestine. There were no differences in body mass and age 
between rats infected and not infected (BODY MASS: 
meanP = 216 g, SdP = 134.1 and meanNP = 275 g; SdNP = 
104.8, respectively; t74 = 1.59; p = 0.114; AGE: medianP = 
3 months; Q1 = 1.8; Q3 = 5.8 and medianNP = 5.2 months, 
Q1 = 3.4; Q3 = 7.1, respectively; U73 = 207; p = 0.07; Fig. 
1b). Mean intensity of infection with N. brasiliensis 
(higher than 200 specimens) was higher in Autumn than in 
the other seasons, but the statistical analysis was not 
carried out because of the low number of individuals para-
sitized (Autumn 2000: 6, Winter 2000: 1, Spring 2000: 0, 
Summer 2000 – 2001: 2, Autumn 2001:0 and Winter 2001: 
1). Syphacia muris was detected in the lower intestine 
and/or caecum-rectum of the host in Autumn. Body mass 
and age did not differ between rats infected and not infec-
ted with this parasite (BODY MASS: meanP = 276 g, SdP = 
97.1; meanNP = 266 g; SdNP = 111.8, respectively; t74 = 0.2; 
p = 0.83; AGE: medianP = 3.5 months; Q1 = 3.1; Q3 = 5.6; 
medianNP = 5 months, Q1 = 3.3; Q3 = 7.1; respectively; U73 
 
 
 
 
128 
= 188; p = 0.36; Fig. 1c). There was no significant 
association between intensity of infection with S. muris 
(mean intensity = 74.28; S = 69.07) and host age (rs = -
0.50; p = 0.25).  
Rats parasitized with H. diminuta were older than non- 
parasitized ones (medianP = 6 months; Q1 = 4.4; Q3 = 9.3 
and medianNP = 4 months, Q1 = 2.9; Q3 = 6.6, respecti-
vely; U73 = 371; p = 0.04; Fig. 1d), and there was a trend to 
have a higher body mass, but differences were not signifi-
cant (meanP = 304 g, SdP = 101.1 and meanNP = 252 g; SdNP 
= 111.55, respectively; t74 = 1.79; p = 0.07). H. diminuta 
was detected in all the seasons studied with a mean in-
tensity of 3.10 per individual (Sd = 3.47).  
In relation with the association among helminths, we ob-
served that the infection with S. muris and N. brasiliensis 
was independent (X2 = 0.23; p = 0.63) and with H. spumosa 
and S. muris was also independent in spite of both last 
species were located in the same portion of the intestine 
(X2 = 0.23; p = 0.63). To difference, H. spumosa and N. 
brasiliensis were negatively associated, and they were 
found in different portions of the intestine (X2 = 7.61; p = 
0.006 Forbes = 0.3125).  
 
Discussion 
 
The endoparasite community of brown rats that inhabiting 
poultry farms of Buenos Aires was characterized by four 
species, being H. spumosa a central species, and N. brasi-
liensis, S. muris and H. diminuta were satellite species. 
As previously noted by Chaunmin et al. (1996) and Sto-
jcevic et al. (2004), the parasitic infection do not affect rat 
survival and growth. The parasitized individuals were 
equal or higher and old, than non-parasitized. Additionally, 
the positive correlation between age of the rats and parasite 
intensity suggests that number of parasites was accumu-
lated during the life of rats, and do not produce mortality 
of the individuals, being host and parasite adapted to each 
other (Anderson, 2000).  
The seasonal variation in the intensity of infection de-
pended on both the characteristics of the hosts and the 
climatic factors. The maximum intensity of infection for H. 
spumosa was occurred in summer, in agreement with the 
greater availability of earthworms that would be important 
in the transmission of this nematode (Anderson, 2000). On 
the other hand, rats had a maximum intensity of N. 
brasiliensis in Autumn. This would be possible because in 
this season occurs the greater precipitation in the study 
area, and N. brasiliensis needs humidity for its survival 
because it does not tolerate desiccation. The infection with 
S. muris only in Autumn, do not have a clear explanation. 
The transmission occurs by means of retroinfection and 
oral infection (direct cycle), so it would not be result of 
climatic factors. Additionally, it is not related to the size or 
age of the host.  The infection would be result of rat 
behaviour such us grooming activities (Anderson, 2000).    
The negative association between H. spumosa and N. bra-
siliensis may be the result of competition between them, or 
the different times of the year when the infection occurs. 
 
Fig. 1. Body mass and age of parasitized (dotted diamond) and no parasitized rats (open diamond) with: a) Heterakis spumosa,  
b) Nippostrongylus brasiliensis, c) Syphacia muris and d) Hymenolepis diminuta.  
 
 
 
 
129
However, the first alternative is less probable because 
these species are located in different parts of the host, 
minimizing the interaction.  
Among the helminth species detected, H. diminuta has 
importance to human health, due to produced gastrointesti-
nal malaise, weakness and lack of appetite. In addition, the 
frequent presence of insects in poultry farms, enhance the 
probability that this parasite completes its cycle. 
This study shows data of the community of helminths in 
rats in relationship with age and weight of their host, being 
one of the scarce studies made with those details. 
 
Acknowledgements 
 
We want to thank all the farmers who kindly let us work at 
their farms; to Graciela Navone, Celina Digiani and Cecilia 
Carballo who help in the determinations of helminths; to 
Emiliano Muschetto for help in the manipulations of intes-
tines and the sources of financial support: University of 
Buenos Aires and National Council of Scientific and 
Technologic Research (CONICET) grants (UBACYT TX 
58 and PIP 548/98). 
 
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ACCEPTED  JUNE 6, 2008 
 
 
 
 


Helminth communities and host-parasite relationships in argentine brown rat (Rattus norvegicus)

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Helminth communities and host-parasite relationships in argentine brown rat (Rattus norvegicus)

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