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Variations in the excretion patterns of helminth eggs in two sympatric mouse lemur species (Microcebus murinus and M. ravelobensis) in northwestern Madagascar

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Abstract

Many factors can influence the parasite load of animal hosts, but integrative studies that simultaneously investigate several factors are still rare in many taxonomic groups. This study investigates the influence of host species, host population density, parasite transmission mode, sex, and two temporal (month, year) factors on gastrointestinal parasite prevalence and fecal egg counts of two endemic primate species from Madagascar, Microcebus ravelobensis and Microcebus murinus. A total of 646 fecal samples were available and analyzed from three dry seasons. Six different helminth egg morphotypes were found, and these were Subulura sp. (14.51 % prevalence), strongyle eggs (12.95 %), Ascaris sp. (7.94 %), Lemuricola sp. (0.17 %), and two forms of tapeworms (Hymenolepis spp.) (1.73 and 0.69 %). Coinfection with more than one egg type was observed in 21.22 % of the samples containing eggs. Multivariate analyses revealed that host species and sex did neither explain significant variation in the prevalence and fecal egg counts of parasites with direct life cycles (Ascaris sp., strongyle egg type, Lemuricola sp.) nor of arthropod-transmitted parasites (Subulura sp.). However, fecal egg counts of Subulura sp. differed significantly between study sites, and the prevalence of Subulura sp. and of parasites with direct life cycles was influenced by temporal parameters, mainly by differences between study years and partly between months. When comparing the findings with the yearly and seasonal rainfall patterns in the area, most results are in accordance with the hypothesis of an increased vulnerability of the host toward infection under some sort of environmental challenge.

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Acknowledgments

We would like to thank the Malagasy government, Ministère De L’Environnement et des Forêts, and Madagascar National Parks (MNP) for their permission to work in the Ankarafantsika National Park and for their support during fieldwork. We are grateful to Solofonirina Rasoloharijaona, Blanchard Randrianambinina, and Romule Rakotondravony from the University of Mahajanga for continuous support during all stages of our work in Madagascar. We thank Sandra Thorén, Miriam Linnenbrink, Alida I.F. Hasiniaina, and Lisette Leliveld for collecting fecal samples, and Jhonny Kennedy and Jean de la Croix for guide services. The Durrell Wildlife Preservation Trust is acknowledged for providing the climate data of Ampijoroa. We furthermore thank Elke Zimmermann and the Institute of Zoology for long-term support and Sandra Buschbaum for technical support during fecal analyses.

Compliance with ethical standards

The authors declare that they have no conflict of interest with regard to this publication. The study was partly funded by the DFG (U.R., Ra 502/9) and by NSF Dissertation Improvement Grant (S.E.K., #0961779), PEO Scholar Award (S.E.K.), the Animal Behavior Society (S.E.K.), Lewis and Clark Fund of the American Philosophical Society (S.E.K.), American Society of Primatologists (S.E.K.), Sigma Xi (National Chapter, S.E.K., grant #G2009101504), Sigma Xi (Arizona State University chapter, S.E.K.), Arizona State University Graduate and Professional Student Association (S.E.K.), and the Arizona State University School of Human Evolution and Social Change (S.E.K.).

All field handling and sampling procedures accorded to the legal requirements of Madagascar and were approved by the Ministry of Water and Forests. All chosen approaches conform to the accepted principles of animal welfare in experimental science and the principles defined in the European Convention for the Protection of Vertebrate Animals used for Experimental and Other Scientific Purposes and its appendix were followed. Furthermore, the methods complied with international ethical standards for the treatment of primates and with the national laws and research rules formulated by the Malagasy authorities.

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Authors and Affiliations

  1. Institute of Zoology, University of Veterinary Medicine Hanover, Buenteweg 17, 30559, Hanover, Germany

    Ute Radespiel, K. Schaber & S. E. Kessler

  2. Arizona State University, Tempe, AZ, USA

    S. E. Kessler

  3. Institute for Biostatistics, Leibniz University Hanover, Hanover, Germany

    F. Schaarschmidt

  4. Institute of Parasitology, University of Veterinary Medicine Hanover, Hanover, Germany

    C. Strube

  5. Department of Anthropology, McGill University, Montreal, Canada

    S. E. Kessler

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  1. Ute Radespiel
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Correspondence to Ute Radespiel.

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Radespiel, U., Schaber, K., Kessler, S.E. et al. Variations in the excretion patterns of helminth eggs in two sympatric mouse lemur species (Microcebus murinus and M. ravelobensis) in northwestern Madagascar. Parasitol Res 114, 941–954 (2015). https://doi.org/10.1007/s00436-014-4259-0

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