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Comparative community-level associations of helminth infections and microparasite shedding in wild long-tailed macaques in Bali, Indonesia

Published online by Cambridge University Press:  24 September 2014

JUSTIN J. S. WILCOX ,
KELLY E. LANE-DEGRAAF ,
AGUSTIN FUENTES  and
HOPE HOLLOCHER
JUSTIN J. S. WILCOX*
Affiliation:
Department of Biological Sciences, Galvin Life Sciences, University of Notre Dame, Notre Dame, IN 46556, USA
KELLY E. LANE-DEGRAAF
Affiliation:
Department of Biological Sciences, Galvin Life Sciences, University of Notre Dame, Notre Dame, IN 46556, USA Department of Biological and Physical Sciences, Fontbonne University, St. Louis, MO 63105, USA
AGUSTIN FUENTES
Affiliation:
Department of Anthropology, University of Notre Dame, Notre Dame, IN 46556, USA
HOPE HOLLOCHER
Affiliation:
Department of Biological Sciences, Galvin Life Sciences, University of Notre Dame, Notre Dame, IN 46556, USA
*
*Corresponding author: Department of Biological Sciences, Galvin Life Sciences, University of Notre Dame, Notre Dame, IN 46556, USA. E-mail: jwilcox2@nd.edu
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Summary

Helminthes have the capacity to modulate host immunity, leading to positive interactions with coinfecting microparasites. This phenomenon has been primarily studied during coinfections with a narrow range of geo-helminthes and intracellular microparasites in human populations or under laboratory conditions. Far less is known regarding differences in coinfection dynamics between helminth types, the range of microparasites that might be affected or the overall community-level effects of helminth infections on microparasites in wild systems. Here, we analysed the presence/absence and abundance patterns of enteric parasites in long-tailed macaques (Macaca fascicularis) on the island of Bali, Indonesia, to assess whether naturally occurring helminth infections were associated with increased shedding of the most common intracellular (Cryptosporidium spp., Isospora spp.) and extracellular (Entamoeba spp., Giardia spp.) microparasites. We also comparatively assessed the statistical correlations of different helminth taxa with microparasite shedding to determine if there were consistent relationships between the specific helminth taxa and microparasites. Helminth infections were associated with increased shedding of both intracellular and extracellular microparasites. Platyhelminthes repeatedly displayed strong positive correlations with several microparasites; while nematodes did not. Our results indicate that helminthes can influence microparasite community shedding dynamics under wild conditions, but that trends may be driven by a narrow range of helminthes.

Keywords

Coinfectionhelminthmicroparasitemacaqueprotozoa
Type
Research Article
Information
Parasitology , Volume 142 , Issue 3 , March 2015 , pp. 480 - 489
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Copyright
Copyright © Cambridge University Press 2014 

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References

REFERENCES

Anderson, R. M., and May, R. M. (1978). Regulation and stability of host–parasite population interactions. I. Regulatory processes. The Journal of Animal Ecology 47, 219–247.CrossRefGoogle Scholar
Bednarska, M., Bajer, A., and Sinski, E. (2008). Cryptosporidium parvum: the course of Cryptosporidium parvum infection in C57BL/6 mice co-infected with the nematode Heligmosomoides bakeri. Experimental Parasitology 120, 21–28.Google Scholar
Behnke, J. M., Bajer, A., Sinski, E., and Wakelin, D. (2001). Interactions involving intestinal nematodes of rodents: experimental and field studies. Parasitology 122(S1), S39–S49.Google Scholar
Bradley, J. E., and Jackson, J. A. (2004). Immunity, immunoregulation and the ecology of trichuriasis and ascariasis. Parasite Immunology 26, 429–441.CrossRefGoogle ScholarPubMed
Bray, J. H., & Maxwell, S. E. (1982). Analyzing and interpreting significant MANOVAs. Review of Educational Research 52, 340–367.CrossRefGoogle Scholar
Brooker, S. J., Pullan, R. L., Gitonga, C. W., Ashton, R. A., Kolaczinski, J. H., Kabatereine, N. B., and Snow, R. W. (2012). Plasmodium–helminth coinfection and its sources of heterogeneity across east Africa. Journal of Infectious Diseases 205, 841–852.Google Scholar
Carvalho, L., Sun, J., Kane, C., Marshall, F., Krawczyk, C., and Pearce, E. J. (2009). Review series on helminths, immune modulation and the hygiene hypothesis: mechanisms underlying helminth modulation of dendritic cell function. Immunology 126, 28–34.CrossRefGoogle ScholarPubMed
Diniz, L. M., Magalhaes, E. F. L., Pereira, F. E. I., Deitze, R., and Ribeiro-Rodrigues, R. (2010). Presence of intestinal helminths decreases T helper type 1 responses in tuberculoid leprosy patients and may increase the risk for multi-bacillary leprosy. Clinical and Experimental Immunology 161, 142–150.CrossRefGoogle ScholarPubMed
Ezenwa, V. O., and Jolles, A. E. (2011). From Host Immunity to Pathogen Invasion: the effects of helminth coinfection on the dynamics of microparasites. Integrative and Comparative Biology 51, 540–551.Google Scholar
Ezenwa, V. O., Etienne, R. S., Luikart, G., Beja-Pereira, A., and Jolles, A. E. (2010). Hidden consequences of living in a wormy world: nematode induced immune suppression facilitates tuberculosis invasion in African buffalo. The American Naturalist 176, 613–624.CrossRefGoogle Scholar
Farid, A., Al-Sherbiny, M., Osman, A., Mohamed, N., Saad, A., Shata, M. T., Lee, D. M., Prince, A. M. and Strickland, G. T. (2005). Schistosoma infection inhibits cellular immune responses to core HCV peptides. Parasite Immunology 27, 189–196.CrossRefGoogle ScholarPubMed
Fenton, A. (2008). Worms and germs: the population dynamic consequences of microparasite–macroparasite co-infection. Parasitology 135, 1545.Google Scholar
Fenton, A., Lamb, T., and Graham, A. L. (2008). Optimality analysis of Th1/Th2 immune responses during microparasite–macroparasite co-infection, with epidemiological feedbacks. Parasitology 135, 841–853.Google Scholar
Fietta, P. and Desante, G. (2009). The effector T-helper cell triade. Rivista di Biologia 102, 61–74.Google Scholar
Fuentes, A., Southern, M., and Suaryana, K. G. (2005). Monkey forests and human landscapes: is extensive sympatry sustainable for Homo sapiens and Macaca fascicularis in Bali? In Commensalism and conflict: the primate–human interface (ed. Patterson, J. and Wallace, J.), pp. 168–195. American Society of Primatology Publications, Norman, OK, USA.Google Scholar
Garcia, L. S., Bruckner, D. A., Brewer, T. C., and Shimizu, R. Y. (1983). Techniques for the recovery and identification of Crypotosporidium oocysts from stool specimens. Journal of Clinical Microbiology 18, 185–190.CrossRefGoogle ScholarPubMed
Graham, A. L. (2008). Ecological rules governing helminth–microparasite coinfection. Proceedings of the National Academy of Sciences 105, 566–570.Google Scholar
Geiger, S. M., Alexander, N. D. E., Fujiwara, R. T., Brooker, S., Cundill, B., Diemert, D. J., Correa-Oliveira, R., and Bethony, J. M. (2011). Necator americanus and helminth co-infections: further down-modulation of hookworm-specific Type 1 immune responses. PLoS Neglected Tropical Diseases, 5, e1280.CrossRefGoogle ScholarPubMed
Haase, R. F., & Ellis, M. V. (1987). Multivariate analysis of variance. Journal of Counseling Psychology 34, 404.CrossRefGoogle Scholar
Hagel, I., Cabrera, M., Puccio, F., Santaella, C., Buvat, E., Infante, B., Zabala, M., Cordero, R., and Di Prisco, M. C. (2011). Co-infection with Ascaris lumbricoides modulates protective immune responses against Giardia duodenalis in school Venezuelan rural children. Acta Tropica 117, 189–195.Google Scholar
Hamer, G. L., Anderson, T. K., Berry, G. E., Makohon-Moore, A. P., Crafton, J. C., Brawn, J. D., Dolinsk, A. C., Krebs, B. L., Ruiz, M. O., Muzzal, P. M., Goldberg, T. L., and Walker, E. D. (2013). Prevalence of filarioid nematodes and trypanosomes in American robins and house sparrows, Chicago USA. International Journal for Parasitology: Parasites and Wildlife, 2, 42–49.Google ScholarPubMed
Hamm, D. M., Agossow, A., Gantin, R. G., Kocherschneidt, L., Banla Dietz, K., and Sloboslay, P. T. (2009). Coinfections with Schistosoma haematobium, Necator americanus, and Entamoeba histolytica/Entamoeba dispar in Children: chemokine and cytokine responses and changes after antiparasite treatment. Journal of Infectious Diseases 199, 1583–1591.Google Scholar
Hartgers, F. C., Obeng, B. B., Kruize, Y. C., Dijkhuis, A., McCall, M., Sauerwein, R. W., Luty, A. J. F., BoaKye, D. and Yazdanbakhsh, M. (2009). Responses to malarial antigens are altered in helminth-infected children. Journal of Infectious Diseases 199, 1528–1535.Google Scholar
Holmes, J. C. (1961). Effects of concurrent infections on Hymenolepis diminuta (Cestoda) & Moniliformis dubius (Acanthocephala). I. General effects and comparison with crowding. The Journal of Parasitology 47, 209–216.Google Scholar
Hewitson, J. P., Grainger, J. R., and Maizels, R. M. (2009). Helminth immunoregulaton: the role of parasite secreted proteins in modulating host immunity. Molecular and Biochemical Parasitology 167, 1–11.CrossRefGoogle ScholarPubMed
Jolles, A. E., Ezenwa, V. O., Etienne, R. S., Turner, W. C., and Olff, H. (2008). Interactions between macroparasites and microparasites drive infection patterns in free-ranging African buffalo. Ecology 89, 2239–2250.Google Scholar
Jones-Engel, L., Engel, G. A., Schillaci, M. A., Froehlich, J., Paputungan, U., & Kyes, R. C. (2004). Prevalence of enteric parasites in pet macaques in Sulawesi, Indonesia. American Journal of Primatology 62, 71–82.Google Scholar
Klotz, C., Ziegler, T., Figueiredo, A. S., Rausch, S., Hepworth, M. R., Obsivac, N., Sers, C., Lang, R., Hammerstein, P., Lucius, R. and Hartmann, S. (2011). A helminth immunomodulator exploits host signaling events to regulate cytokine production in macrophages. PLoS Pathogens 7, e1001248.Google Scholar
Knowles, S. C. (2011). The effect of helminth co-infection on malaria in mice: a meta-analysis. International Journal for Parasitology 41, 1041–1051.CrossRefGoogle ScholarPubMed
Knox, D. P. (2007). Proteinase inhibitors and helminth parasite infection. Parasite Immunology 29, 57–71.Google Scholar
Lagrue, C., and Poulin, R. (2008). Intra- and interspecific competition among helminth parasites: effects on Coitocaecum parvum life history strategy, size and fecundity. International Journal for Parasitology 38, 1435–1444.CrossRefGoogle ScholarPubMed
Lane, K. E., Lute, M., Rompis, A., Wandia, I. N., Putra, I. A., Hollocher, H., and Fuentes, A. (2010). Pests, pestilence, and people: the long-tailed macaque and its role in the cultural complexities of Bali. In Indonesian Primates (ed. Gursky-Doyen, S. and Supriatna, J.), pp. 235–248. Springer, New York.Google Scholar
Lane, K. E., Holley, C., Hollocher, H., and Fuentes, A. (2011). The anthropogenic environment lessens the intensity and prevalence of gastrointestinal parasites in Balinese long-tailed macaques (Macaca fascicularis). Primates 52, 117–128.Google Scholar
Lane-deGraaf, K. E., Putra, I. G. A., Wandia, I. N., Rompis, A., Hollocher, H., and Fuentes, A. (2014). Human behavior and opportunities for parasite transmission in communities surrounding long-tailed macaque populations in Bali, Indonesia. American Journal of Primatology 76, 159–167.CrossRefGoogle ScholarPubMed
Loudon, J. E., Howells, M. E., and Fuentes, A. (2006). The importance of integrative anthropology: a preliminary investigation employing primatological and cultural anthropological data collection methods in assessing human-monkey co-existence in Bali, Indonesia. Ecological and Environmental Anthropology 26, 1–13.Google Scholar
MacIntosh, A. J., Hernandez, A. D., and Huffman, M. A. (2010). Host age, sex, and reproductive seasonality affect nematode parasitism in wild Japanese macaques. Primates 51, 353–364.Google Scholar
Maizels, R. M., Balic, A., Gomez-Escobar, N., Nair, M., Taylor, M. D., and Allen, J. E. (2003). Helminth parasites: masters of regulations. Immunological Reviews 201, 89–116.Google Scholar
Marcogliese, D. J., and Pietrock, (2011). Combined effects of parasites and contaminants on animal health: parasites do matter. Trends in Parasitology 27, 123–130.Google Scholar
Moreno, P. G., Eberhardt, M. A. T., Lamattina, D., Previtali, M. A., and Beldomenico, P. M. (2013). Intra-phylum and inter-phyla associations among gastrointestinal parasites in two wild mammal species. Parasitology Research 112, 3295–3304.Google Scholar
Nacher, M., Singhasivanont, P., Yimsamrant, S., Manibunyongt, W., Thanyavanicht, N., Wuthisent, P., and Looareesuwant, S. (2002). Intestinal helminth infections are associated with increased incidence of Plasmodium falciparum infection. Journal of Parasitology 88, 55–58.Google Scholar
Nunn, C. L. (2012). Primate disease ecology in comparative and theoretical perspective. American Journal of Primatology 74, 497–509.CrossRefGoogle ScholarPubMed
Oros, M., Hanzelová, V., and Scholz, T. (2009). Tapeworm Khawiasinensis: review of the introduction and subsequent decline of a pathogen of carp, Cyprinus carpio . Veterinary Parasitology 164, 217–222.Google Scholar
Pedersen, A. B., and Fenton, A. (2007). Emphasizing the ecology in parasite community ecology. Trends in Ecology and Evolution 22, 133–139.CrossRefGoogle ScholarPubMed
Petney, T. N. and Andrews, R. H. (1998). Multiparasite communities in animals and humans: frequency, structure, and pathogenic significance. International Journal for Parasitology 28, 377–393.CrossRefGoogle ScholarPubMed
Philippe, H., Lartillot, N., and Brinkmann, H. (2005). Multigene analyses of bilaterian animals corroborate the monophyly of Ecdysozoa, Lophotrochozoa, and Protostomia. Molecular Biology and Evolution 22, 1246–1253.Google Scholar
Poulin, R., and Morand, S. (2000). The diversity of parasites. Quarterly Review of Biology, 277–293.Google Scholar
Resende, T., Hirsch, C. S., Toossi, Z. and Dietze, R., Ribeiro-Rodrigues, R. (2007) Intestinal helminth co-infection has a negative impact on both anti-Mycobacterium tuberculosis immunity and clinical response to tuberculosis therapy. Clinical and Experimental Immunology 147, 45–52.Google Scholar
Reyes, J. L., Terrazas, C. A., Alonso-Trujillo, J., van Rooijen, N., Satoskar, A. R., and Terrazas, L. I. (2010). Early removal of alternatively activated macrophages leads to Taenia crassiceps cysticercosis clearance in vivo . International Journal for Parasitology 40, 731–742.CrossRefGoogle ScholarPubMed
Reyes, J. L., Espinoza-Jiménez, A. F., González, M. I., Verdin, L., and Terrazas, L. I. (2011). Taenia crassiceps infection abrogates experimental autoimmune encephalomyelitis. Cellular Immunology 267, 77–87.CrossRefGoogle ScholarPubMed
Robinson, M. W., Dalton, J. P., O'Brien, B. A., and Donnelly, S. (2013). Fasciola hepatica: the therapeutic potential of a worm secretome. International Journal for Parasitology 43, 283–291.Google Scholar
Romagnani, S. (1997). The Th1/Th2 paradigm. Immunology Today 18, 263–266.Google Scholar
SAS Institute Inc. 2011. Base SAS® 9·3 Procedures Guide. Cary, NC: SAS Institute Inc.Google Scholar
Southern, M. W. (2002). An assessment of potential habitat corridors and landscape ecology for long-tailed Macaques (Macaca fascicularis) on Bali, Indonesia. Doctoral dissertation, Central Washington University.Google Scholar
Spector, P. E. (1977). What to do with significant multivariate effects in multivariate analyses of variance. Journal of Applied Psychology 62, 158.Google Scholar
Steinmann, P., Utzinger, J., Du, Z. W., and Zhou, X. N. (2010). Multiparasitism: a neglected reality on global, regional and local scale. Advances in Parasitology 73, 21–50.Google Scholar
Sutherland, W. J., Freckleton, R. P., Godfray, H. C. J., Beissinger, S. R., Benton, T., Cameron, D. D., Caramel, Y., Coomes, D., Couson, T., Emmerson, M. C., Hails, R. S., Hays, G. C., Hodgeson, D. J., Hutchings, M. J., Johnson, D., Jones, J. P. G., Keeling, M. J., Kokko, H., Kunin, W. E., Lambin, X., Lweis, O. T., Mahli, Y., Mieszjowska, N., Milner-Gulland, E. J., Norris, K., Phillmore, A. B., Purves, D. W., Reid, J. M., Reuman, D. C., Thompson, K., et al. (2013). Identification of 100 fundamental ecological questions. Journal of Ecology 101, 58–67.Google Scholar
Taraschewski, H. (2006). Hosts and parasites and aliens. Journal of Helminthology 80, 99–128.Google Scholar
Terrazas, C. A., Gómez-García, L., and Terrazas, L. I. (2010). Impaired pro-inflammatory cytokine production and increased Th2-biasing ability of dendritic cells exposed to Taenia excreted secreted antigens: a critical role for carbohydrates but not for STAT6 signaling. International Journal for Parasitology 40, 1051–1062.Google Scholar
Thomas, P. G., and Harn, D. A. (2004). Immune biasing by helminth glycans. Cellular Microbiology 6, 13–22.Google Scholar
Wang, M. L., Cao, Y. M., Luo, E. J., Zhang, Y., and Guo, Y. J. (2013). Pre-existing Schistosoma japonicum infection alters the immune response to Plasmodium berghei infection in C57BL/6 mice. Malaria Journal 12, 322.Google Scholar
Warton, D. I., and Hudson, H. M. (2004). A MANOVA statistic is just as powerful as distance-based statistics, for multivariate abundances. Ecology 85, 858–874.Google Scholar
Weyher, A. H., Ross, C., and Semple, S. (2006). Gastrointestinal parasites in crop raiding and wild foraging Papio anubis in Nigeria. International Journal of Primatology 27, 1519–1534.Google Scholar