Hostname: page-component-78c5997874-8bhkd Total loading time: 0 Render date: 2024-11-15T01:53:47.980Z Has data issue: false hasContentIssue false
  • English
  • Français

Gastrointestinal helminth fauna of rodents from Cambodia: emphasizing the community ecology of host–parasite associations

Published online by Cambridge University Press:  01 December 2016

K. Chaisiri ,
M. Chou ,
C.C. Siew ,
S. Morand  and
A. Ribas
K. Chaisiri*
Affiliation:
Department of Helminthology, Faculty of Tropical Medicine, Mahidol University, Thailand
M. Chou
Affiliation:
Rodolphe Mérieux Laboratory of Cambodia and Faculty of Pharmacy, University of Health Sciences, Phnom Penh, Cambodia
C.C. Siew
Affiliation:
Detection and Diagnostic Laboratories, DSO National Laboratories, Singapore
S. Morand
Affiliation:
Department of Helminthology, Faculty of Tropical Medicine, Mahidol University, Thailand CNRS Institut des Sciences de l'Evolution – CIRAD Animal et Gestion Intégrée des Risques, Centre d'Infectiologie Christophe Mérieux du Laos, Vientiane, Laos
A. Ribas
Affiliation:
Section of Parasitology, Department of Biology, Healthcare and the Environment, Faculty of Pharmacy and Food Sciences, University of Barcelona, Spain
*
*E-mail: kittipong.cha@mahidol.ac.th
Get access Rights & Permissions [Opens in a new window]

Abstract

Extensive field surveys of rodents were conducted in Cambodia from 2008 to 2014 to study the diversity and ecology of helminth infection in wild rodent populations. Gastrointestinal helminths were isolated from 14 species of rodents (569 individuals) trapped from different habitats (forest, dry land, rain-fed land and human settlements) in four provinces of Cambodia (Krong Preah Sihanouk, Mondolkiri, Pursat and Steung Treng). The average prevalence of parasitic infection was 58.5% (range, 16.0–64.7%), and 19 helminth taxa were identified in total. Trichostrongylid nematodes were the most prevalent (25.8%), followed by Raillietina sp. (14.1%), Gongylonema neoplasticum (10.7%), Syphacia muris (9.8%) and Hymenolepis diminuta (9.6%). Potential rodent-borne zoonotic helminths were also identified, and the risks of helminthiasis were discussed. The status of helminth infection and species diversity in rodents from settlements were significantly lower than in rodents from forest and peri-domesticated habitats, which indicates that habitat alteration might affect helminth infection and diversity in rodent hosts. Generalized linear models revealed that host attributes (host species and maturity) and environmental factors (habitat and geographical location) were explanatory variables for helminth infection in these rodents. Using network analyses, we showed that the oriental house rat, Rattus tanezumi, was the most central host in the rodent–helminth assemblage, based on the number of helminth taxa it shared with other rodent species. Therefore, R. tanezumi could play an important role in rodent–helminth interactions and helminth transmission to other rodent hosts.

Type
Research Papers
Information
Journal of Helminthology , Volume 91 , Issue 6 , November 2017 , pp. 726 - 738
Copyright
Copyright © Cambridge University Press 2016 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Almeida-Neto, M., Guimaraes, P., Guimaraes, P.R., Loyola, R.D. & Ulrich, W. (2008) A consistent metric for nestedness analysis in ecological systems: reconciling concept and measurement. Oikos 117, 1227–1239.Google Scholar
Anderson, R.C., Chabaud, A.G. & Willmott, S. (2009) Keys to the nematode parasites of vertebrates. Archival Volume. Wallingford, CAB International.Google Scholar
Aplin, K.P., Brown, P.R., Jacob, J., Krebs, C. & Singleton, G.R. (2003) Field methods for rodent studies in Asia and the Indo-Pacific. Canberra, ACIAR Monograph No. 100.Google Scholar
Atmar, W. & Patterson, B.D. (1993) The measure of order and disorder in the distribution of species in fragmented habitat. Oecologia 96, 373–382.Google Scholar
Bastolla, U., Fortuna, M.A., Pascual-García, A., Ferrera, A., Luque, B. & Bascompte, J. (2009) The architecture of mutualistic networks minimizes competition and increases biodiversity. Nature 458, 1018–1021.Google Scholar
Bates, D., Mächler, M., Bolker, B.M. & Walker, S.C. (2015) Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67, 1–48.Google Scholar
Behnke, J.M., Lewis, J.W., Zain, S.N. & Gilbert, F.S. (1999) Helminth infections in Apodemus sylvaticus in southern England: interactive effects of host age, sex and year on the prevalence and abundance of infections. Journal of Helminthology 73, 31–44.Google Scholar
Blasdell, K., Bordes, F., Chaisiri, K., Chaval, Y., Claude, J., Cosson, J.F., Latinne, A., Michaux, J., Morand, S., Pagès, M. & Tran, A. (2015) Progress on research on rodents and rodent-borne zoonoses in South-east Asia. Wildlife Research 42, 98–107.Google Scholar
Bordes, F. & Morand, S. (2008) Helminth species diversity of mammals: parasite species richness is a host species attribute. Parasitology 135, 1701–1705.Google Scholar
Bordes, F., Morand, S., Pilosof, S., Claude, J., Krasnov, B.R., Cosson, J.F., Chaval, Y., Ribas, A., Chaisiri, K., Blasdell, K., Herbreteau, V., Dupuy, S. & Tran, A. (2015) Habitat fragmentation alters the properties of a host–parasite network: rodents and their helminths in South-East Asia. Journal of Animal Ecology 84, 1253–1263.Google Scholar
Burnham, K.P. & Anderson, D.R. (2002) Model selection and multimodel inference: A practical information-theoretic approach. 2nd edn. New York, Springer International.Google Scholar
Calcagno, V. & De Mazancourt, C. (2010) glmulti: an R package for easy automated model selection with (generalized) linear models. Journal of Statistical Software 1, 1–29.Google Scholar
Chaisiri, K., Chaeychomsri, W., Siruntawineti, J., Bordes, F., Herbreteau, V. & Morand, S. (2010) Human-dominated habitats and helminth parasitism in Southeast Asian murids. Parasitology Research 107, 931–937.Google Scholar
Chaisiri, K., Morand, S. & Ribas, A. (2011) Notocotylus loeiensis n. sp. (Trematoda: Notocotylidae) from Rattus losea (Rodentia: Muridae) in Thailand. Parasite 18, 35–38.Google Scholar
Chaisiri, K., Chaeychomsri, W., Siruntawineti, J., Ribas, A., Herbreteau, V. & Morand, S. (2012) Diversity of gastrointestinal helminths among murid rodents from northern and northeastern Thailand. Southeast Asian Journal of Tropical Medicine and Public Health 43, 21–28.Google ScholarPubMed
Chaisiri, K., Siribat, P., Ribas, A. & Morand, S. (2015) Potentially zoonotic helminthiases of murid rodents from the Indo-Chinese Peninsula: impact of habitat and the risk of human infection. Vector-Borne and Zoonotic Diseases 15, 73–85.Google Scholar
Claveria, F.G., Causapin, J., Guzman, M.A., Toledo, M.G. & Salibay, C. (2005) Parasite biodiversity in Rattus spp. caught in wet markets. Southeast Asian Journal of Tropical Medicine and Public Health 36, 146–148.Google Scholar
Coker, R.J., Hunter, B.M., Rudge, J.W., Liverani, M. & Hanvoravongchai, P. (2011) Emerging infectious diseases in Southeast Asia: regional challenges to control. Lancet 377, 599–609.Google Scholar
Corbet, G. & Hill, J. (1992) The mammals of the Indomalayan region: a systematic review. Oxford, Natural History Museum Publications and Oxford University Press.Google Scholar
Csardi, G. & Nepusz, T. (2006) The igraph software package for complex network research. International Journal of Computer Systems, 1695. Available at http://igraph.sf.net (accessed 16 August 2016).Google Scholar
Dallas, T. & Presley, S.J. (2014) Relative importance of host environment, transmission potential, and host phylogeny to the structure of parasite metacommunities. Oikos 123, 866–874.Google Scholar
De Bellocq, J.G., Sarà, M., Casanova, J.C., Feliu, C. & Morand, S. (2003) A comparison of the structure of helminth communities in the woodmouse, Apodemus sylvaticus, on islands of the western Mediterranean and continental Europe. Parasitology Research 90, 64–70.Google Scholar
Dormann, C.F., Fruend, J., Bluethgen, N. & Gruber, B. (2009) Indices, graphs and null models: analyzing bipartite ecological networks. The Open Ecology Journal 2, 7–24.CrossRefGoogle Scholar
Froeschke, G. & Matthee, S. (2014) Landscape characteristics influence helminth infestations in a peri-domestic rodent – implications for possible zoonotic disease. Parasites & Vectors 7, 393.Google Scholar
Godfrey, S.S. (2013) Networks and the ecology of parasite transmission: a framework for wildlife parasitology. International Journal for Parasitology: Parasites and Wildlife 2, 235–245.Google ScholarPubMed
Herbreteau, V., Jittapalapong, S., Rerkamnuaychoke, W., Chaval, Y., Cosson, J.F. & Morand, S. (2011) Protocols for field and laboratory rodent studies. Bangkok, Kasetsart University Press.Google Scholar
Joppa, L.N., Montoya, J.M., Solé, R., Sanderson, J. & Pimm, S.L. (2010) On nestedness in ecological networks. Evolutionary Ecology Research 12, 35–46.Google Scholar
Kindt, R. & Coe, R. (2005) Tree diversity analysis: A manual and software for common statistical methods for ecological and biodiversity studies. Nairobi, World Agroforestry Centre (ICRAF).Google Scholar
Krishnasamy, M., Singh, K.I., Ambu, S. & Ramachandran, P. (1980) Seasonal prevalence of the helminth fauna of the wood rat Rattus tiomanicus (Miller) in West Malaysia. Folia Parasitologica 27, 231–235.Google Scholar
Macnish, M.G., Morgan-Ryan, U.M., Monis, P.T., Behnke, J.M. & Thompson, R.C.A. (2002) A molecular phylogeny of nuclear and mitochondrial sequences in Hymenolepis nana (Cestoda) supports the existence of a cryptic species. Parasitology 125, 567–575.Google Scholar
Marshall, J.T. (1988) Family Muridae: rats and mice. pp. 397–487 in Lekagul, B. & McNeely, J.A. (Eds) Mammals of Thailand. Bangkok, Association for the Conservation of Wildlife.Google Scholar
McKinney, M.L. (2008) Effects of urbanization on species richness: a review of plants and animals. Urban Ecosystem 11, 161–176.Google Scholar
McQuaid, C.F. & Britton, N.F. (2013) Host-parasite nestedness: a result of co-evolving trait-values. Ecological Complexity 13, 53–59.Google Scholar
Meerburg, B.G., Singleton, G.R. & Kijlstra, A. (2009) Rodent-borne diseases and their risks for public health. Critical Reviews in Microbiology 35, 221–270.Google Scholar
Mohd Zain, S.N., Behnke, J.M. & Lewis, J.W. (2012) Helminth communities from two urban rat populations in Kuala Lumpur, Malaysia. Parasites & Vectors 5, 5–47.CrossRefGoogle ScholarPubMed
Morand, S., Jittapalapong, S., Supputamongkol, Y., Abdullah, M.T. & Huan, T.B. (2014a) Infectious diseases and their outbreaks in Asia-Pacific: biodiversity and its regulation loss matter. PLoS One 9, e90032. doi:10.1371/journal.pone.0090032.Google Scholar
Morand, S., McIntyre, M. & Baylis, M. (2014b) Domesticated animals and human infectious diseases of zoonotic origins: domestication time matters. Infection, Genetics and Evolution 24, 76–81.Google Scholar
Morand, S., Bordes, F., Blasdell, K., Pilosof, S., Cornu, J.F., Chaisiri, K., Chaval, Y., Cosson, J.F., Claude, J., Feyfant, T., Herbreteau, V., Dupuy, S. & Tran, A. (2015a) Assessing the distribution of disease-bearing rodents in human-modified tropical landscapes. Journal of Applied Ecology 52, 784–794.Google Scholar
Morand, S., Jittapalapong, S. & Kosoy, M. (2015b) Rodents as hosts of infectious diseases: biological and ecological characteristics. Vector-Borne and Zoonotic Diseases 15, 1–2.Google Scholar
Oksanen, J., Blanchet, F.G., Kindt, R., Legendre, P., Minchin, P.R., O'Hara, R.B., Simpson, G.L., Solymos, P., Stevens, M.H. & Wagner, H. (2013) Vegan: Community ecology package. R package version 2.0-10. Available at http://CRAN.R-project.org/package=vegan (accessed 16 August 2016).Google Scholar
Opsahl, T. (2009) Structure and evolution of weighted networks. London, University of London (Queen Mary College).Google Scholar
Pagès, M., Chaval, Y., Herbreteau, V., Waengsothorn, S., Cosson, J.F., Hugot, J.P., Morand, S. & Michaux, J. (2010) Revisiting the taxonomy of the Rattini tribe: a phylogeny-based delimitation of species boundaries. BMC Evolutionary Biology 10, 184.Google Scholar
Pakdeenarong, N., Siribat, P., Chaisiri, K., Douangboupha, B., Ribas, A., Chaval, Y., Herbreteau, V. & Morand, S. (2014) Helminth communities in murid rodents from southern and northern localities in Lao PDR: the role of habitat and season. Journal of Helminthology 88, 302–309.CrossRefGoogle ScholarPubMed
Palmeirim, M., Bordes, F., Chaisiri, K., Siribat, P., Ribas, A. & Morand, S. (2014) Helminth parasite species richness in rodents from Southeast Asia: role of host species and habitat. Parasitology Research 113, 3713–3726.CrossRefGoogle ScholarPubMed
Paramasvaran, S., Krishnasamy, M., Lee, H.L., John, J., Lokman, H., Naseem, B.M., Rehana, A.S. & Santhana, R.J. (2005) Helminth infections in small mammals from Ulu Gombak Forest Reserve and the risk to human health. Tropical Biomedicine 22, 191–194.Google Scholar
Pham, X.D., Tran, C.L. & Hasegawa, H. (2001) Helminths collected from Rattus spp. in Bac Ninh Province, Vietnam. Comparative Parasitology 68, 261–264.Google Scholar
Pilosof, S., Fortuna, M., Cosson, J.F., Galan, M., Ribas, A., Chaisiri, K., Segal, E., Krasnov, B.R., Morand, S. & Bascompte, J. (2014) Host–parasite network structure is associated with community-level immunogenetic diversity. Nature Communication 5, 5172. doi: 10.1038/ncomms6172.Google Scholar
Pilosof, S., Morand, S., Krasnov, B.R. & Nunn, C.L. (2015) Potential parasite transmission in multi-host networks based on parasite sharing. PLoS One 10. doi: 10.1371/journal.pone.0117909.Google Scholar
Poulin, R. (2010) Network analysis shining light on parasite ecology and diversity. Trends in Parasitology 26, 492–498.Google Scholar
Prasetyo, R.H. (2016) Survey of house rat intestinal parasites from Surabaya district, east Java, Indonesia that can cause opportunistic infections in humans. Southeast Asian Journal of Tropical Medicine and Public Health 47, 194–198.Google Scholar
R Core Team (2015) R: A language and environment for statistical computing. Vienna, R Foundation for Statistical Computing. Available at http://www.R-project.org/ (accessed 27 August 2016).Google Scholar
Ribas, A., Veciana, M., Chaisiri, K. & Morand, S. (2012) Protospirura siamensis n. sp. (Nematoda: Spiruridae) from rodents in Thailand. Systematic Parasitology 82, 21–27.Google Scholar
Roberts, M. (1991) The parasites of the Polynesian rat within and beyond New Zealand. International Journal of Parasitology 21, 777–783.Google Scholar
Rossin, M.A., Malizia, A.I., Timi, J.T. & Poulin, R. (2010) Parasitism underground: determinants of helminth infections in two species of subterranean rodents (Octodontidae). Parasitology 137, 1569–1575.Google Scholar
Schmidt, G.D. (1986) Handbook of tapeworm identification. Florida, Boca Raton, CRC Press.Google Scholar
Singh, M. & Chee-Hock, C. (1971) On a collection of nematode parasites from Malayan rats. Southeast Asian Journal of Tropical Medicine and Public Health 2, 516–522.Google Scholar
Singleton, G.R., Hinds, L.A., Krebs, C.J. & Spratt, D.M. (2003) Rats, mice and people: rodent biology and management. Canberra, Australian Center for International Agriculture Research.Google Scholar
Singleton, G.R., Belmain, S., Brown, P.R., Aplin, K. & Htwe, N.M. (2010) Impacts of rodent outbreaks on food security in Asia. Wildlife Research 37, 355–359.Google Scholar
Sinniah, B. (1979) Parasites of some rodents in Malaysia. Southeast Asian Journal of Tropical Medicine and Public Health 10, 115–121.Google Scholar
Skrjabin, K.I., Shikhobalova, N.P. & Orlov, I.V. (1970) Trichocephalidae and Capillariidae of animals and man and the diseases caused by them. Jerusalem, Weiner Bindery Ltd.Google Scholar
Timi, J.T. & Poulin, R. (2003) Parasite community structure within and across host populations of a marine pelagic fish: how repeatable is it? International Journal of Parasitology 33, 1353–1362.Google Scholar
Tubangui, M.A. (1931) Trematode parasites of Philippine vertebrates, II: two Echinostome flukes from rats. Philippine Journal of Science 44, 273.Google Scholar
Van der Mescht, L., Krasnov, B.R., Matthee, C.A. & Matthee, S. (2016) Community structure of fleas within and among populations of three closely related rodent hosts: nestedness and beta-diversity. Parasitology 143, 1268–1278.Google Scholar
Veciana, M., Chaisiri, K., Morand, S. & Ribas, A. (2012) Helminths of the Asian house shrew Suncus murinus from Cambodia. Cambodian Journal of Natural History 2, 115–122.Google Scholar
Veciana, M., Chaisiri, K., Morand, S., Miquel, J. & Ribas, A. (2013) New biogeographical and morphological information on Physaloptera ngoci Le-Van-Hoa, 1961 (Nematoda: Physalopteridae) in Southeast Asian rodents. Parasite 20, 23.Google Scholar
Veciana, M., Bain, O., Morand, S., Chaisiri, K., Douangboupha, B., Miquel, J. & Ribas, A. (2015) Breinlia (Breinlia) jittapalapongi n. sp. (Nematoda: Filarioidea) from the Asian house rat Rattus tanezumi Temminck in Lao PDR. Systematic Parasitology 90, 237–245.Google Scholar
Walther, B.A. & Morand, S. (1998) Comparative performance of species richness estimation methods. Parasitology 116, 395–405.CrossRefGoogle ScholarPubMed
Wiroreno, W. (1978) Nematode parasites of rats in west Java, Indonesia. Southeast Asian Journal of Tropical Medicine and Public Health 9, 520–525.Google Scholar
Wright, D.H. & Reeves, J.H. (1992) On the meaning and measurement of nestedness of species assemblages. Oecologia 92, 416.CrossRefGoogle ScholarPubMed
Yamaguti, S. (1958) The Digenetic trematodes of vertebrates part I: volume I. pp. 800–972 in Yamaguti, S. (Ed.) Systema Helminthum. New York, Interscience Publishers.Google Scholar