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ORIGINAL PAPER
Human-dominated habitats and helminth parasitism
in Southeast Asian murids
Kittipong Chaisiri &Win Chaeychomsri &
Jindawan Siruntawineti &Frédéric Bordes &
Vincent Herbreteau &Serge Morand
Received: 14 May 2010 / Accepted: 7 June 2010 /Published online: 1 July 2010
#Springer-Verlag 2010
Abstract The effect of habitat anthropization is investigated
using a comparative analysis based on a literature survey of
the gastrointestinal helminths of murid rodents described in
Southeast Asia (SEA). The literature survey gave 30
references on helminth diversity concerning 20 murid rodent
species. The diversity of helminths was high with a total of
13 species of cestodes, 15 species of trematodes, 29 species
of nematodes and one species of acanthocephalans. The
highest helminth species richness was found in Rattus
tanezumi,Rattus norvegicus and Rattus argentiventer,all
these species were found in more human-dominated habitats
(agricultural areas or human settlements). Helminth species
richness was positively linked across rodent species to the
level of the anthropization of the host environment from
forests, agricultural areas to human settlements.
Introduction
Many parts of the world are currently suffering high
dramatic environmental changes (Acevedo-Whitehouse
and Duffus 2009) in relation to human activities and their
associated ecological impacts. Habitat modification is one
of these changes that can alter biological systems, and
consequently, the epidemiological environment (Daily and
Ehrlich 1996). Unfortunately, our understanding on how
habitat may affect host–parasite dynamics in wild mammals
is virtually unexplored.
Many studies have tried to link, sometimes successfully,
host specific traits to helminth species richness with still
contradictory results (Arneberg 2002; Bordes et al. 2007,
2008,2009,2010; Lindenfors et al. 2007; Morand and
Harvey 2000; Nunn et al. 2003; Poulin 1995). One reason
that could explain the lack of general patterns emerging
from these studies may be related to the lack of inves-
tigations of host environment effects on parasite diversity.
Moreover, while determinants of helminth species richness
have been extensively explored across mammal species
(Bordes et al. 2009,2010; Morand and Poulin 1998), few
studies have specifically focused on rodents (but see
(Bordes et al. 2007; Feliu et al. 1997)).
Among mammals, rodents are the most abundant group
with more than 2,700 species worldwide (i.e. 42% of
mammalian species on Earth) (Wilson and Reeder 2005),
living successfully in many environments throughout the
world. Two thirds of rodent species belong to the family
Muridae, which also represents most of the rodents found
in Asia (Aplin et al. 2003). According to (Wilson and
Reeder 2005), 263 mammal species and 35 murine species
are recognised in SEA. Although there were several
K. Chaisiri
Department of Helminthology, Faculty of Tropical Medicine,
Mahidol University,
Bangkok 10400, Thailand
K. Chaisiri :W. Chaeychomsri :J. Siruntawineti
Department of Zoology, Faculty of Science, Kasetsart University,
Bangkok 10900, Thailand
F. Bordes :S. Morand
Institut des Sciences de l’Evolution, UMR 5554 CNRS-IRD-
UM2, CC65, Université de Montpellier 2,
Montpellier 34095, France
V. Herbreteau :S. Morand (*)
UR22 AGIRs CIRAD, Campus International de Baillarguet,
Montpellier 34398, France
e-mail: serge.morand@univ-montp2.fr
Parasitol Res (2010) 107:931–937
DOI 10.1007/s00436-010-1955-2
comparative studies concerning helminth species richness
in rodents in Europe and North America (Bordes et al.
2007; Feliu et al. 1997), studies in SEA still remained very
limited.
In SEA, rodent species show some specificity to the
habitat and particularly in relation to the habitat used by
humans, such as primary forests, agricultural areas or
human settlements (Adler 2009; Adler et al. 1999;
Jittapalapong et al. 2009,2010; Suntsov et al. 2003).
We reviewed research articles investigating gastrointes-
tinal helminths of murid rodents in SEA in order to provide
an updated global view of rodent–parasite relationships in
this part of the world. More precisely, our main aims were
(1) to reveal parasite richness according to rodent host
species and countries prospected and (2) to explore the
influence of habitat on helminth richness.
Materials and methods
Parasitic data
This study scopes previous reports of macroparasites in murid
rodents in SEA. Among macroparasites, we focused on
helminths present in the gastrointestinal tract. We found
concordant references from the database of the Natural
History Museum in London, UK (www.nhm.ac.uk), and
websites (especially www.pubmed.com and www.science
direct.com). We retrieved these references by using key-
words linked to rodent taxonomy (i.e. all genus and species
names, including their synonyms, as described by (Wilson
and Reeder 2005)
Data on rodents
We extracted from these references the number of rodent
hosts and the number of countries investigated for each
helminth species. We also recorded the total number of
countries where each rodent species is described according to
the International Union for Conservation of Nature and
Natural Resources (IUCN) Red List (http://www.iucnred list.
org/)(Table1). We calculated the range of each species using
the ArcGIS 9.3 (ESRI, Redlands, CA, USA) based on the
distribution maps realised by the Southeast Asian Mammal
Databank project (SAMD) database (Boitani et al. 2006).
These maps correspond to those produced by the IUCN. The
habitats of rodent species were ranked according to the
degree of human habitat use following (Jittapalapong et al.
2008,2009), from primary and secondary forests (Index 1),
agricultural areas (Index 2) and human settlements (i.e.
cities, villages, houses) (Index 3). Information on the habitat
used by the rodents came from (Jittapalapong et al. 2008,
2009; but see also Suntsov et al. 2003). We found
information on the rodent geographic distribution across
SEA, rodent body mass, and habitat from Lekagul and
McNeely (1977), (Aplin et al. 2003; Corbet and Hill 1992;
Wilson and Reeder 2005)(Table1).
Phylogenetic tests
To avoid phylogenetic influences when investigating
patterns of parasite species richness (Morand and Poulin
2003), we tested our predictions using the independent
contrasts method (Felsenstein 1985). The phylogenetic infor-
mation came from (Pagès et al. 2010). The phylogenetic tree
Table 1 Helminth infection and rodent characteristics: regional distribution and anthropization index of habitat
Rodent species Number of helminth
species identified
Number of rodents
examined
Number of countries
present
b
Range
(sq. km)
a
Anthropization
index
Bandicota indica 10 35 6 1660810 2
Berylmys bowersi 7 46 6 919457 1
Leopoldamys sabanus 8 188 6 2069742 1
Maxomys surifer 6 183 8 2329340 1
Maxomys whiteheadi 2 70 4 1075249 1
Niviventer cremoriventer 4 37 4 1016541 1
Rattus argentiventer 15 373 10 1788618 2
Rattus exulans 13 654 11 3810398 3
Rattus losea 5 9 5 553573 2
Rattus norvegicus 22 1,782 10 4030357 3
Rattus tanezumi 34 1,183 10 4030269 3
Rattus tiomanicus 12 483 5 1212916 2
a
According to IUCN Red List (http://www.iucnredlist.org/) and SAMD project (Boitani et al. 2006)
b
According to Lekagul and McNeely (1977), (Corbet and Hill 1992)
932 Parasitol Res (2010) 107:931–937
of rodents was completely resolved (no polytomies). Contrasts
were calculated using the CAIC software (Purvis and
Rambaut 1995). To confirm the proper standardisation of
contrasts, we regressed the absolute values of standardised
contrasts against their standard deviations. We found no
positive relationships suggesting that it was not necessary to
transform the branch lengths before computing the standard
deviations (Garland et al. 1992). Contrasts were then analysed
using standard parametric tests with all correlations between
contrasts forced through the origin (Garland et al. 1992).
Statistical analysis
First, we performed general regression modelling on raw
data to explain helminth species richness with the number
of hosts sampled and the index of anthropization as
independent variables. In this analysis, the index of
anthropization was used as a qualitative variable. Second,
we performed multiple regression analysis forced through
the origin using independent contrasts on all precedent
variables. The helminth species richness was analysed as
the dependent variable with the number of hosts sampled
and the index of anthropization as independent variables. In
this analysis, the index of anthropization was used as a
semi-quantitative variable. The number of host sampled
was log-transformed before the analyses.
Results
Diversity of helminths in rodents
We found 30 references dealing with helminth species
richness in Southeast Asian rodents across six countries:
Indonesia, Malaysia, Myanmar, the Philippines, Thailand
and Vietnam. We found no surveys from Brunei, Cambo-
dia, Lao People's Democratic Republic, Papua New
Guinea, Singapore and Timor. The studies included,
altogether, 20 rodent species and 58 parasite species,
including 13 cestodes, 15 trematodes, 29 nematodes and
one acanthocephalan (Table 2). We grouped in Rattus
tanezumi into six species that are now considered as
synonyms according to the latest taxonomy (Wilson and
Reeder 2005), i.e. Rattus rattus,Rattus rattus diardii,
Rattus rattus flavipectus,Rattus rattus molliculus,Rattus
rattus sladeni, and Rattus rattus tanezumi. The highest
values of total helminth species richness were found in R.
tanezumi (34), Rattus norvegicus (22) and R. argentiventer
(15). In comparison, the study of (Feliu et al. 1997)included
only five murine rodent species of the West Palearctic
(Apodemus sylvaticus, M. domesticus, M. spretus, R. rattus
and R. norvegicus) with helminth species richness varying
from 11 to 28.
Relationship between parasite diversity and anthropization
index
According to the anthropization ranking and the classifica-
tion of rodent species to three categories, we obtained 524
rodent individuals in forested areas, 900 in agricultural areas
and 3,619 in human settlements (Table 1). Using raw data,
we performed a multiple regression analysis and found that
helminth species richness was significantly explained by the
number the index of anthropization (P=0.05), but not by the
host sample size and the host geographical range (F
3,8
=
7.797, R=0.86, P<0.01). We then performed a forward
selection to select significant variables. The host geograph-
ical range and host sample size were not found to be
correlated with the helminth species richness (P>0.05). The
anthropization was significantly selected as a significant
determinant of the helminth species richness (F
1,10
=17.228,
R=0.80, P= 0.002). The increasing helminth species richness
was observed from rodents living in the forest (Index 1), to
agricultural areas (Index 2) and human settlements (Index 3)
using ANOVA (F
2,9
=7.757, P=0.01) (Fig.1a).
Similar results were observed using the independent
contrasts method and then controlling for the potential
phylogenetic confounding effects (P<0.01). Again, a
helminth species richness was positively related to the host
sample size (P= 0.004) and the anthropization ranking
(P=0.03). An increased helminth species richness was
positively linked with the index of anthropization (Fig. 1b).
Discussion
Helminth species richness: geographical patterns and limits
of available samplings
Murid rodents in SEA are infected with various helminth
parasites. Species with the greatest range harbour a higher
diversity of helminths, as shown by R. norvegicus and R.
tanezumi, which are present throughout SEA. The extent of
the home range creates unprecedented contacts with other
animal niches and may result in acquiring new parasites.
The highest number of helminth species was reported from
Vietnam (28) followed by Malaysia (25), Thailand (17),
Indonesia (10), the Philippines (9) and Myanmar (1).
However, the literature does not cover all Southeast Asian
countries since no rodent investigation seemed to have been
done in Brunei, Cambodia, Lao People's Democratic
Republic, Papua New Guinea, Singapore and Timor. More
importantly, several rodent species have never been
investigated for helminths, such as Chiromyscus chiropus,
Hapalomys longicaudatus, Chiropodomys gliroides, Chiro-
podomys major, Berylmys berdmorei, Mus pahari, Mus
shortridgei, Mus cervicolor, Mus cookii, Niviventer hin-
Parasitol Res (2010) 107:931–937 933
poon, Maxomys baeodon and Lenothrix canus.These
species are mainly rodents living in forests or rare species,
but their role in the maintenance of parasites and transmis-
sion to other rodents might also be investigated. The
number of individual rodents investigated for helmintho-
logical surveys also showed this bias with lower host
sample size in rodents living in forests compared to rodent
species living in more human-dominated habitats. More-
over, difficulties in identifying rodents still occur as attested
by misnamed rodents. Rodent taxonomy is under revision
especially with the R. rattus complex in which some
species are hardly distinguishable (Pagès et al. 2010).
Finally, this review reveals that the number of individual
hosts investigated is non-equal according to the phylum or
class of parasites surveyed. Some hosts have been investi-
gated for only one phylum or class of parasites and there
are very few or no information on the total parasite
community in rodent species. Problems of parasite identi-
Table 2 Number of helminth species (cestodes, trematodes, nematodes and acanthocephalans) found in Southeast Asian rodent species
Number of different helminth species identified
Rodent species
Cestodes
Trematodes
Nematodes
Acanthocephalans
Total
References
Bandicota indica 423 1 10 (1), (18), (19), (22), (24), (26)
Bandicota savilei 110 0 2 (2), (24)
Berylmys bowersi 106 0 7 (18), (20), (22), (25)
Leopoldamys edwardsi 101 0 2 (18), (22)
Leopoldamys sabanus 008 0 8 (6), (25), (26), (27), (30)
Maxomys surifer 303 0 6 (9), (14), (18), (22)
Maxomys whiteheadi 002 0 2 (6), (25), (29)
Mus caroli 200 0 2 (18)
Mus musculus 121 0 4 (4), (13), (27), (31)
Niviventer cremoriventer 004 0 4 (6), (25), (30)
Niviventer fulvescens 101 0 2 (18), (22)
Rattus andamanensis 400 0 4 (18)
Rattus argentiventer 2 2 10 1 15 (8), (21), (24), (25), (26),
Rattus exulans 624 1 13 (1), (2), (7), (11), (23), (26), (30)
Rattus hoffmanni 001 0 1 (6)
Rattus losea 014 0 5 (22)
Rattus nitidus 115 0 7 (18), (19), (22)
Rattus norvegicus 849 1 22 (1), (2), (3), (16), (17), (26), (28)
Synonyms of Rattus tanezumi
Rattus rattus 553 0 13 (1), (2), (3), (5), (11), (15), (16), (17)
Rattus rattus diardii 349 1 17 (12), (26)
Rattus rattus flavipectus 110 0 2 (18), (19)
Rattus rattus molliculus 101 0 2 (18), (22)
Rattus rattus sladeni 025 0 7 (19), (22)
Rattus rattus tanezumi 103 1 5 (21)
Rattus tiomanicus 307 1 12 (10), (14), (20), (26)
Reference note: (1) Areekul and Radomyos, 1970; (2) Chenchittikul et al., 1983; (3) Claveria et al., 2005; (4) Coombs and Crompton,
1991; (5) Cross and Basaca, 1986; (6) Hasegawa and Syafruddin, 1994; (7) Hasegawa and Syafruddin, 1995; (8)
Hasegawa et al., 1992; (9) Kamiya et al., 1987; (10) Krishnasamy et al., 1980; (11) Krivolutsky et al., 1991; (12)
Leong et al., 1979; (13) Maleewong et al., 1988; (14) Miyazaki and Dunn, 1965; (15) Monzon and Kitikoon, 1989;
(16) Nama, 1990; (17) Namue and Wongsawad, 1997; (18) Nguyen, 1986; (19) Nguyen, 1991; (20) Paramasvaran et
al., 2005; (21) Pham, 2001; (22) Phan, 1984; (23) Roberts, 1991; (24) Sey, 2001; (25) Singh and Chee-Hock, 1971;
(26) Sinniah, 1979; (27) Sukontason et al., 1999; (28) Tubangui, 1931; (29) Varughese, 1973; (30) Wiroreno, 1978;
(31) Won
g
aswad et al., 1998
934 Parasitol Res (2010) 107:931–937
fication also occurred and express the needs to develop
molecular tools and to improve morphological and molec-
ular identification in further studies.
Determinants of helminth species richness in murid rodents
in SEA: anthropogenic influences?
Some patterns of helminth richness seem to emerge.
Multiple regression analyses showed that the number of
examined hosts and the index of the anthropization
significantly explain the number of helminth species
harboured by a host species. Increased helminth species
richness was found to be associated with rodents living in
anthropogenic areas. Our results give new support to the
recent idea that anthropogenic factors may alter parasite
communities or host–parasite relationships (i.e. agrochem-
icals, (Rohr et al. 2008); pollutants, (Bull et al. 2006);
eutrophization of aquatic systems, (Johnson and Carpenter
2008)). However, despite recent progresses linking human
activities and parasitism, our understanding of how habitat
alteration can alter host–parasite relationships in terrestrial
ecosystems is still rather limited (but see (Gillespie and
Chapman 2008; Gillespie et al. 2005), for parasitism in
primates living in logged and fragmented forests compare to
undisturbed forests). Importantly, our study is then one of the
few that supports the emerging idea that parasite species
richness may be greater for mammals in human-altered
habitats (Gillespie and Chapman 2008; Gillespie et al. 2005).
(Suntsov et al. 2003) showed a trend of decreasing rodent
species richness and increasing rodent abundances along a
gradient of disturbance from primary tropical forest to
human villages. The increase in helminth species richness
can be linked to an increase of rodent abundance in more
human-dominated habitat, as host abundance (and host
density) is a potential determinant of parasite species
richness (Morand and Poulin 1998; Poulin and Morand
2004). Such an increase in parasite species richness in
human-dominated habitats could be related, at least theoret-
ically, to some variation in host exposure and/or host
susceptibility to parasites. Modification of host exposure to
parasites could be mediated by new host ranging patterns or
host densities in disturbed habitats. Smaller home ranges
could lead hosts to use habitat intensively, increasing the
level of host infection by infective stages of parasites, but
also favouring host contacts (Kuenzi et al. 2001). Smaller
home ranges could then be linked to higher parasite species
richness as it was recently established across mammals
(Bordes et al. 2009). Moreover, an increase in host densities
in disturbed habitats or in smaller home ranges could also
promote higher host contacts and then parasite transmissions.
Host exposure to parasites could also increase due to longer
persistence of infective stages in disturbed habitats. Hosts
could also become more susceptible to parasites in anthro-
pogenic habitats due to impaired immune defences via
nutritional stress or pollutants. Taken together, all these
mechanisms could explain that disturbed habitats seem to be
associated with higher helminth species richness in rodents
leading to higher zoonotic risks.
Suggestions to improve rodent parasitism studies in SEA
If this literature survey has brought interesting preliminary
information on helminths of murid rodents in SEA, it also
clearly identifies limits of current available data. The main
limits may be related to limited or totally absent surveys for
some rodent species or in some countries and also non-
standardised collections of parasites.
We then suggest (1) improving sampling effort by
collecting in a standardised way all helminth taxa on all
rodent species in every SEA countries, (2) identifying
parasites with molecular confirmation, (3) focusing partic-
ularly on rodent species or populations of the same species
that live under different degrees of habitat alteration. Taken
together, all these suggestions should certainly improve our
Fig. 1 Effect of anthropization (using the index of anthropization) on
helminth species richness (a) using raw data (residuals from covariant,
P=0.001) and (b) using independent contrasts (F
1,12
=5.69, R= 0.58;
P=0.03)
Parasitol Res (2010) 107:931–937 935
knowledge of the potential impacts of anthropogenic
habitat disturbance on parasitic infections in wild popula-
tions and it will help at determining sources of infection
and ways of transmission between rodent species or
between rodents and humans and their domesticated
animals (Meerburg et al. 2009).
Acknowledgements This study is supported by the French ANR
Biodiversity (ANR 07 BDIV 012, project CERoPath) “Community
Ecology of Rodents and their Pathogens in a Changing Environment”.
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