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Tracking year-to-year changes in intestinal nematode communities of rufous mouse lemurs (Microcebus rufus)


While it is known that intestinal parasite communities vary in their composition over time, there is a lack of studies addressing how variation in component communities (between-hosts) manifests in infracommunities (within-host) during the host lifespan. In this study, we investigate the changes in the intestinal parasite infracommunities in wild-living rufous mouse lemurs (Microcebus rufus) from Ranomafana National Park in southeastern Madagascar from 2010 to 2012. We used high-throughput barcoding of the 18S rRNA gene to interrogate parasite community structure. Our results show that in these nematode communities, there were two frequently occurring putative species and four rarer putative species. All putative species were randomly distributed over host individuals and they did not occur in clear temporal patterns. For the individuals caught in at least two different years, there was high turnover of putative species and high variation in fecal egg counts. Our study shows that while there was remarkable variation in infracommunities over time, the component community was relatively stable. Nevertheless, the patterns of prevalence varied substantially between years in each component community.

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* Corresponding author. Institute of Biotechnology, University of Helsinki, P.O. Box 56, FI-00014 Helsinki, Finland. E-mail:
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Alizon, S. (2013). Parasite co-transmission and the evolutionary epidemiology of virulence. Evolution 67, 921933.
Anderson, R. C., Chabaud, A. G. and Willmott, S. (2009). Keys to the Nematode Parasites of Vertebrates, 1st Edn. CAB International, Wallingford, UK.
Atsalis, S. (2008). A Natural History of the Brown Mouse Lemur. Pearson Education, Upper Saddle River, NJ, USA.
Baermann, G. (1917). Eine einfache methode zur auffindung von Ankylostomum (Nematoden) larven in erdproben. Tijdschrid Ergeneeskd 57, 131137.
Balmer, O. and Caccone, A. (2008). Multiple-strain infections of Trypanosoma brucei across Africa. Acta Tropica 107, 275279.
Balmer, O. and Tanner, M. (2011). Prevalence and implications of multiple-strain infections. Lancet Infectious Diseases 11, 868878.
Barnes, E. M. (1970). Effect of hibernation intestinal flora. The American Journal of Clinical Nutrition 23, 15191524.
Bates, D., Maechler, M., Bolker, B. and Walker, S. (2014). lme4: linear mixed-effects models using Eigen and S4. R package version 1.1–7.
Behnke, J. M., Bajer, A., Harris, P. D., Newington, L., Pidgeon, E., Rowlands, G., Sheriff, C., Kuliś-Malkowska, K., Siński, E., Gilbert, F. S. and Barnard, C. J. (2008 a). Temporal and between-site variation in helminth communities of bank voles (Myodes glareolus) from N.E. Poland. 2. The infracommunity level. Parasitology 135, 9991018.
Behnke, J. M., Bajer, A., Harris, P. D., Newington, L., Pidgeon, E., Rowlands, G., Sheriff, C., Kuliś-Malkowska, K., Siński, E., Gilbert, F. S. and Barnard, C. J. (2008 b). Temporal and between-site variation in helminth communities of bank voles (Myodes glareolus) from N.E. Poland. 1. Regional fauna and component community levels. Parasitology 135, 985997.
Bhadury, P. and Austen, M. C. (2010). Barcoding marine nematodes: an improved set of nematode 18S rRNA primers to overcome eukaryotic co-interference. Hydrobiologia 641, 245251.
Blaxter, M., Mann, J., Chapman, T., Thomas, F., Whitton, C., Floyd, R. and Abebe, E. (2005). Defining operational taxonomic units using DNA barcode data. Philosophical Transactions of the Royal Society B: Biological Sciences 360, 19351943.
Bouma, H. R., Carey, H. V. and Kroese, F. G. M. (2010). Hibernation: the immune system at rest? Journal of Leukocyte Biology 88, 619624.
Bush, A. O., Lafferty, K. D., Lotz, J. M. and Shostak, A. W. (1997). Parasitology meets ecology on its own terms: Margolis et al. revisited. The Journal of Parasitology 83, 575583.
Callait, M. and Gauthier, D. (2000). Parasite adaptations to hibernation in Alpine marmots (Marmota marmota). In Life in the Cold (ed. Heldmaier, G. and Klingenspor, M.), pp. 139146. Springer-Verlag, Berlin.
Carey, H. V. (1990). Seasonal changes in mucosal structure and function in ground squirrel intestine. American Journal of Physiology – Regulatory, Integrative and Comparative Physiology 259, R385R392.
Carey, H. V., Pike, A. C., Weber, J. L., Turner, A. K., Visser, S. C., Beijer-Liefers, H. R., Bouma, H. R. and Kroese, F. G. M. (2012). Impact of hibernation on gut microbiota and intestinal barrier function in ground squirrels. In Living in a Seasonal World: Thermoregulatory and Metabolic Adaptations (ed. Ruf, T., Bieber, C., Arnold, W. and Millesi, E.), pp. 281291. Springer, Heidelberg, Germany.
Chute, R. M. (1960). Overwintering of helminths in hibernating animals. Journal of Parasitology, 46, 539.
Clutton-Brock, T. H. and Pemberton, J. M. (2004). Individuals and populations. In Soay Sheep: Dynamics and Selection in an Island Population (ed. Clutton-Brock, T. H. and Pemberton, J. M.), pp. 116. CUP, Cambridge, UK.
Coggings, J. R., Tedesco, J. L. and Ruppercht, C. E. (1982). Seasonal changes and overwintering of parasites in the bat, Myotis lucifugus (Le Conte), in a Wisconsin hibernaculum. American Midland Naturalist 107, 305315.
Conover, W. J. (1999). Practical Nonparametric Statistics, 3rd Edn. John Wiley & Sons, Hoboken, NJ, USA.
Craig, B. H., Pilkington, J. G. and Pemberton, J. M. (2006). Gastrointestinal nematode species burdens and host mortality in a feral sheep population. Parasitology 133, 485496.
Craig, B. H., Jones, O. R., Pilkington, J. G. and Pemberton, J. M. (2009). Re-establishment of nematode infra-community and host survivorship in wild Soay sheep following anthelmintic treatment. Veterinary Parasitology 161, 4752.
Dausmann, K. H., Glos, J., Ganzhorn, J. U. and Heldmaier, G. (2005). Hibernation in the tropics: lessons from a primate. Journal of Comparative Physiology B: Biochemical, Systems, and Environmental Physiology 175, 147155.
De Roij, J. and MacColl, A. D. C. (2012). Consistent differences in macroparasite community composition among populations of three-spined sticklebacks, Gasterosteus aculeatus L. Parasitology 139, 14781491.
Dobson, A. (1986). Inequalities in the individual reproductive success of parasites. Parasitology 92, 675682.
Dove, A. D. M. and Cribb, T. H. (2006). Species accumulation curves and their applications in parasite ecology. Trends in Parasitology 22, 568574.
Dreyer, G., Fernandes-Silva, E., Alves, S., Rocha, A., Albuquerque, R. and Addiss, D. (1996). Patterns of detection of Strongyloides stercoralis in stool specimens: implications for diagnosis and clinical trials. Journal of Clinical Microbiology 34, 25692571.
Dubey, J. P., Moura, L., Majumdar, D., Sundar, N., Velmurugan, G. V., Kwok, O. C. H., Kelly, P., Krecek, R. C. and Su, C. (2009). Isolation and characterization of viable Toxoplasma gondii isolates revealed possible high frequency of mixed infection in feral cats (Felis domesticus) from St Kitts, West Indies. Parasitology 136, 589594.
Ebbert, M. A., McGrew, W. C. and Marchant, L. F. (2013). Community composition, correlations among taxa, prevalence, and richness in gastrointestinal parasites of baboons in Senegal, West Africa. Primates 54, 183189.
Edgar, R. C., Haas, B. J., Clemente, J. C., Quince, C. and Knight, R. (2011). UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27, 21942200.
Fenton, A., Viney, M. E. and Lello, J. (2010). Detecting interspecific macroparasite interactions from ecological data: patterns and process. Ecology Letters 13, 606615.
Fenton, A., Knowles, S. C. L., Petchey, O. L. and Pedersen, A. (2014). The reliability of observational approaches for detecting interspecific parasite interactions: comparison with experimental results. International Journal of Parasitology 44, 437445.
Gau, R. J., Kutz, S. and Elkin, B. T. (1999). Parasites in grizzly bears from the central Canadian Arctic. Journal of Wildlife Diseases 35, 618621.
Gibbons, L. M., Jacobs, D. E., Fox, M. T. and Hansen, J. (2014). The RVC/FAO Guide to Veterinary Diagnostic Parasitology.
Gillespie, T. R. (2006). Noninvasive assessment of gastrointestinal parasite infections in free-ranging primates. International Journal of Primatology 27, 11291143.
Gotelli, N. J. and Colwell, R. K. (2001). Quantifying biodiversity: procedures and pitfalls in the measurement and comparison of species richness. Ecology Letters 4, 379391.
Grenfell, B. T., Wilson, K., Isham, V. S., Boyd, H. E. and Dietz, K. (1995). Modelling patterns of parasite aggregation in natural populations: trichostrongylid nematode-ruminant interactions as a case study. Parasitology 111 (Suppl.), S135S151.
Griffiths, E. C., Pedersen, A. B., Fenton, A. and Petchey, O. L. (2011). The nature and consequences of coinfection in humans. The Journal of Infection 63, 200206.
Haukisalmi, V., Henttonen, H. and Tenora, F. (1988). Population dynamics of common and rare helminths in cyclic vole populations. Journal of Animal Ecology 57, 807825.
Hayward, A. D. (2013). Causes and consequences of intra- and inter-host heterogeneity in defense against nematodes. Parasite Immunology 35, 362373.
Hayward, A. D., Wilson, A. J., Pilkington, J. G., Pemberton, J. M. and Kruuk, L. E. B. (2009). Ageing in a variable habitat: environmental stress affects senescence in parasite resistance in St Kilda Soay sheep. Proceedings of the Royal Society B: Biological Sciences 276, 34773485.
Højsgaard, S., Halekoh, U. and Yan, J. (2006). The R package geepack for generalized estimating equations. Journal of Statistical Software 15, 111.
Jones, O. R., Crawley, M. J., Pilkington, J. G. and Pemberton, J. M. (2005). Predictors of early survival in Soay sheep: cohort-, maternal- and individual-level variation. Proceedings of the Royal Society B: Biological sciences 272, 26192625.
Klein, S. (2004). Hormonal and immunological mechanisms mediating sex differences in parasite infection. Parasite Immunology 26, 247264.
Kurtz, C. C. and Carey, H. V. (2007). Seasonal changes in the intestinal immune system of hibernating ground squirrels. Developmental and Comparative Immunology 31, 415428.
Liang, K.-Y. and Zeger, S. L. (1986). Longitudinal data analysis using generalized linear models. Biometrika 73, 1322.
Löytynoja, A., Vilella, A. J. and Goldman, N. (2012). Accurate extension of multiple sequence alignments using a phylogeny-aware graph algorithm. Bioinformatics 28, 16841691.
Medlar, A., Aivelo, T. and Löytynoja, A. (2014). Séance: reference-based phylogenetic analysis for 18S rRNA studies. BMC Evolutionary Biology 14, 235.
Nakagawa, S. and Schielzeth, H. (2010). Repeatability for Gaussian and non-Gaussian data: a practical guide for biologists. Biological Reviews of the Cambridge Philosophical Society 85, 935956.
Nishigori, M. (1928). The factors which influence the external development of Strongyloides stercoralis and on auto-infection with this parasite. Journal of Formosan Medical Association 247, 156.
Oksanen, J., Blanchet, F. G., Kindt, R., Legendre, P., Minchin, P. R., O'Hara, R. B., Simpson, G. L., Solymos, P., Stevens, M. H. H. and Wagner, H. (2013). Vegan: Community Ecology Package. R package version 2.0–1o0.
Pilosof, S., Fortuna, M. A., Vinarski, M. V., Korallo-Vinarskaya, N. P. and Krasnov, B. R. (2013). Temporal dynamics of direct reciprocal and indirect effects in a host-parasite network. The Journal of Animal Ecology 82, 987996.
Poulin, R. (1997). Population abundance and sex ratio in dioecious helminth parasites. Oecologia 111, 375380.
Quast, C., Pruesse, E., Yilmaz, P., Gerken, J., Schweer, T., Yarza, P., Peplies, J. and Glöckner, F. O. (2013). The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Research 41, D590D596.
Quince, C., Lanzen, A., Davenport, R. J. and Turnbaugh, P. J. (2011). Removing noise from pyrosequenced amplicons. BMC Bioinformatics 12, 38.
R Core Team (2013). R: a Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.
Raharivololona, B. M. and Ganzhorn, J. U. (2009). Gastrointestinal parasite infection of the gray mouse lemur (Microcebus murinus) in the littoral forest of Mandena, Madagascar: effects of forest fragmentation and degradation. Madagascar Conservation and Development 4, 103112.
Raharivololona, B. and Ganzhorn, J. (2010). Seasonal variations in gastrointestinal parasites excreted by the gray mouse lemur Microcebus murinus in Madagascar. Endangered Species Research 11, 113122.
Revelle, W. (2015). Psych: Procedures for Psychological, Psychometric and Personality Research. R package version 2.0–10.
Rinaldi, L., Maurelli, M. P., Musella, V., Santaniello, A., Coles, G. C. and Cringoli, G. (2010). FLOTAC: an improved method for diagnosis of lungworm infection in sheep. Veterinary Parasitology 11, 395398.
Sambrook, J., Fritsch, E. F. and Maniatis, T. (1989). Molecular Cloning: a Laboratory Manual, 2nd Edn. Cold Spring Harbor Laboratory Press, Long Island, NY, USA.
Sandground, B. J. H. (1926). Biological studies on the life-cycle in the genus Strongyloides grassi, 1879. American Journal of Epidemiology 6, 337388.
Shaw, D. J. and Dobson, A. P. (1995). Patterns of macroparasite abundance and aggregation in wildlife populations: a quantitative review. Parasitology 111, S111S133.
Simitch, T. and Petrovitch, Z. (1954). Ce qu'il advient avec les helminthes du Citellus citellus au cours du sommeil hibernal de ce rongeur. Rivista di Parassitologia 15, 655662.
Sokal, R. R. and Rohfl, F. J. (1995). The Principles and Practice of Statistics in Biological Research, 3rd Edn. W.H. Freeman, New York, USA.
Sonoyama, K., Fujiwara, R., Takemura, N., Ogasawara, T., Watanabe, J., Ito, H. and Morita, T. (2009). Response of gut microbiota to fasting and hibernation in Syrian hamsters. Applied and Environmental Microbiology 75, 64516456.
Stamatakis, A. (2006). RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22, 26882690.
Stear, M. J., Bishop, S. C., Duncan, J. L., Mckellar, Q. A. and Murray, M. (1995). The repeatability of faecal egg counts, peripheral eosinophil counts, and plasma pepsinogen concentrations during deliberate infection with Ostertagia circumcincta . International Journal for Parasitology 25, 375380.
Stear, M. J., Bairden, K., Bishop, S. C., Gettinby, G., Mckellar, Q. A., Park, M., Strain, S. and Wallace, D. S. (1998). The processes influencing the distribution of parasitic nematodes among naturally infected lambs. Parasitology 117, 165171.
Stear, M. J., Singleton, D. and Matthews, L. (2011). An evolutionary perspective on gastrointestinal nematodes of sheep. Journal of Helminthology 85, 113120.
Stephenson, L. S., Latham, M. C. and Ottesen, E. A. (2000). Malnutrition and parasitic helminth infections. Parasitology 121, S23S38.
Telfer, S., Lambin, X., Birtles, R., Beldomenico, P., Burthe, S., Paterson, S. and Begon, M. (2010). Species interactions in a parasite community drive infection risk in a wildlife population. Science 330, 243246.
Uparanukraw, P., Phongsri, S. and Morakote, N. (1999). Fluctuations of larval excretion in Strongyloides stercoralis infection. The American Journal of Tropical Medicine and Hygiene 60, 967973.
Viney, M. E. and Graham, A. L. (2013). Patterns and processes in parasite co-infection. Advances in Parasitology 82, 321369.
Wickham, H. and Chang, W. (2014). ggplot2: an Implementation of the Grammar of Graphics. R package version 1.0.0.
Wilson, K., Grenfell, B. T., Pilkington, J. G., Boyd, H. E. and Gulland, F. M. (2014). Parasites and their impact. In Soay Sheep: Dynamics and Selection in an Island Population (ed. Clutton-Brock, T. H. and Pemberton, J. M.), pp. 113165. Cambridge University Press, Cambridge, UK.
Wood, E. L. D., Matthews, J. B., Stephenson, S., Slote, M. and Nussey, D. H. (2013). Variation in fecal egg counts in horses managed for conservation purposes: individual egg shedding consistency, age effects and seasonal variation. Parasitology 140, 115128.
Wright, P. C. and Andriamihaja, B. (2002). Making a rain forest national park work in Madagascar: Ranomafana National Park and its long-term research commitment. In Making Parks Work: Strategies for Preserving Tropical Nature (ed. Terborgh, J., van Schaik, C., Davenport, L. and Rao, M.), pp. 112136. Island Press, Washington, DC, USA.
Zohdy, S., Gerber, B. D., Tecot, S., Blanco, M. B., Winchester, J. M., Wright, P. C. and Jernvall, J. (2014). Teeth, sex, and testosterone: aging in the world's smallest primate. PLoS ONE 9, e109528.
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