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University of Veterinary Medicine Hannover University of Veterinary Medicine Hannover Patterns of parasitism in wild Verreaux’s sifakas (Propithecus verreauxi) at Kirindy Forest, Madagascar: Assessing the role of host behavior Thesis Submitted in partial fulfillment of the requirements for the degree of Doctor of Veterinary Medicine - Doctor medicinae veterinariae - (Dr. med. vet.) by Andrea Springer Hamburg Hannover 2015 Academic supervision: Prof. Dr. med. vet. Franz-Josef Kaup Pathology Unit German Primate Center 1st referee: Prof. Dr. Franz-Josef Kaup 2nd referee: Prof. Prof. h. c. Dr. Ursula Siebert Day of the oral examination: 13.11.2015 This study was funded by the German Primate Center and the German Research Foundation (Ka 1082/29-1). II For the sifakas of Kirindy Forest III The following parts of this thesis have been submitted for publication in peer-reviewed journals: Chapter 6: Andrea Springer, Alexander Mellmann, C laudia Fichtel and Peter M. Kappeler: “Sociality shapes inter-group transmission of Escherichia coli in a group-living wild primate, Verreaux’s sifaka” Submitted for publication to BMC Ecology (date of submission: 14.07.2015, in review) Chapter 8: Andrea Springer, Claudia Fichtel, Sébastien Calvignac-Spencer, Fabian H. Leendertz and Peter M. Kappeler (2015): “Hemoparasites in a wild primate: Plasmodium and Babesia interact in a lemur species” International Journal for Parasitology: Parasites and Wildlife, in press, doi:10.1016/j.ijppaw.2015.10.006. Furthermore, results of this study have been publicly presented at the following conferences: Ecology and Evolution of Infectious Diseases, May 26 – 29, 2015, Athens, GA, USA: “Hemoparasite infections in a wild primate: Parasite interaction shapes prevalence patterns” (poster), Springer A., Fichtel C., Calvignac-Spencer S., Leendertz F.H., Kappeler P. M. EWDA student workshop “Human Impact on Wildlife Diseases”, March 26 – 30, 2015, Veyrier-du-Lac, France: “Social spread of Escherichia coli through a lemur population” (poster), Springer A., Mellmann A., Fichtel C., Kappeler P.M. IV 10th topical meeting of the Ethological Society: “Causes and Consequences of Social Behavior”, February 11 – 14, 2015, Hamburg, Germany: “Environmental versus social transmission: How Escherichia coli spreads through a lemur population” (talk), Springer A., Fichtel C., Mellmann A., Kappeler P.M. 25th Congress of the International Primatological Society, August 11 – 16, 2014, Hanoi, Vietnam: “Investigating parasite spread through a lemur population” (talk), Springer A., Fichtel C., Leendertz F.H., Calvignac-Spencer S., Mellmann A., Nunn C.L., Kappeler P.M. International Conference on Diseases of Zoo and Wild Animals, May 28 – June 01, 2014, Warsaw, Poland: “Investigating parasite spread through a lemur population” (talk), Springer A., Fichtel C., Leendertz F.H., Calvignac-Spencer S., Mellmann A., Nunn C.L., Kappeler P.M. Göttinger Freilandtage, December 03 – 05, 2013, Göttingen, Germany: “Investigating parasite spread through a lemur population” (talk), Springer A., Fichtel C., Leendertz F.H., Calvignac-Spencer S., Mellmann A., Nunn C.L., Kappeler P.M. International Prosimian Congress, August 05 – 11, 2013, Ranomafana, Madagascar: “Investigating parasite spread through a sifaka population” (talk), Springer A., Fichtel C., Leendertz F.H., Calvignac-Spencer S., Mellmann A., Nunn C.L., Kappeler P.M. V VI Table of Contents List of abbreviations……………………………………………………………………… X Chapter 1 – Introduction………………………………………………………………..... 13 Parasitism – an ecological perspective……………………………………..... 13 Parasitism and behavior……………………………………………………… 13 Chapter 2 – Literature Review………………………………………………………….. 16 Parasitic infections – a major cost of sociality?............................................... 16 Benefits of living in groups………………………………………………. 16 Direct parasite transmission, animal density and social complexity……... 16 Sociality and vector-borne parasites……………………………………… 18 Behavioral adaptations against parasitism…………………………………… 18 Avoidance of fecal contamination………………………………………... 19 Social barriers to parasite transmission…………………………………… 20 Grooming……………………………………………………………......... 21 Linking theory with empirical data: Approaches to studying transmission in the wild………………………………………………………………………. 22 Verreaux’s sifakas as a study system………………………………………… 22 Behavioral ecology……………………………………………………….. 24 Parasites of Verreaux’s sifakas…………………………………………… 25 Chapter 3 – Objectives and Structure of this Thesis…………………………………… 27 Chapter 4 – Materials and Methods……………………………………………………... 29 Study site and study animals……………………………………………….... 29 Remote data collection………………………………………………………. 29 Calculation of home ranges and their overlaps…………………………… 30 Estimation of intergroup encounter rates………………………………..... 30 Behavioral observations……………………………………………………… 30 Invasive sampling…………………………………………………………..... 31 Noninvasive sampling……………………………………………………….. 32 VII Overview of data collection………………………………………………….. 33 Sample processing…………………………………………………………… 33 Microscopy of fecal samples…………………………………………….... 33 Fecal cultures and preparation of helminth larvae for PCR………………. 34 DNA extraction from fecal samples and PCRs…………………………… 35 Escherichia coli isolation and multi-locus sequence-typing……………… 37 Ectoparasites……………………………………………………………… 38 Analysis of blood samples and PCRs for hemoparasites………………..... 38 Phylogenetic analyses………………………………………………………... 40 Statistical analyses…………………………………………………………… 41 Ranging patterns and behavioral data…………………………………..... 41 Nematode infections……………………………………………………… 42 Escherichia coli type sharing……………………………………………... 42 Ectoparasite infections………………………………………………….... 44 Hemoparasite infections………………………………………………….. 44 Chapter 5 – Low diversity of intestinal parasites in an arboreal primate, Verreaux’s sifaka, at Kirindy Forest, Madagascar (Manuscript 1)……………………. 46 Chapter 6 – Sociality shapes inter-group transmission of Escherichia coli in a group- living wild primate, Verreaux’s sifaka (Manuscript 2)…………................. 66 Chapter 7 – Ectoparasites of a group-living wild lemur species, Verreaux’s sifaka: Does sociality influence infection risk? (Manuscript 3) ……....................... 92 Chapter 8 – Hemoparasites in a wild primate: Plasmodium and Babesia interact in a lemur species (Manuscript 4).......................................................................... 111 Chapter 9 – General Discussion…………………………………………………………. 140 Arboreality: a strategy to avoid parasites?....................................................... 142 Social behavior and directly transmitted infections…………………………. 146 Social group size and vector-borne infections………………………………. 151 Inter-specific parasite interactions: an important determinant of infection patterns………………………………………………………………………. 151 VIII Conclusions…………………………………………………………………... 153 Summary…………………………………………………………………………………... 155 Zusammenfassung…………………………………………………………….................... 158 References…………………………………………………………………………………. 161 Acknowledgements………………………………………………………………………... 220 Erklärung………………………………………………………………………………….. 221 IX List of abbreviations °C degree Celsius AIC Akaike Information Criterion ANOVA analysis of variance approx. approximately BLAST Basic Local Alignment Search Tool Bp bootstrapped pseudo-replicates bp basepairs CNFEREF Centre National de Formation, d’Etudes et de Recherche en Environnement et Foresterie cyt b cytochrome b df degrees of freedom DNA deoxyribonucleic acid E. coli Escherichia coli E. dispar Entamoeba dispar E. histolytica Entamoeba histolytica E. nuttalli Entamoeba nuttalli e.g. for example EMBL European Molecular Biology Laboratory ESBL extended-spectrum beta-lactamases EUCAST European Committee on Antimicrobial Susceptibility Testing F-EA formalin-ethylacetat FEC fecal egg count g gram GLMM generalized linear mixed model GPS global positioning system h hours ha hectare i.e. that means ID identity ITS internal transcribed spacer X LMM linear mixed model MALDI-ToF matrix-assisted laser desorption ionization time-of-flight mass-spectrometry MgCl2 magnesium chloride min minutes ml milliliter MLST multi-locus sequence typing mM millimolar MR-QAP multiple regression quadratic assignment procedure N sample size NLR neutrophil : lymphocyte ratio no. number p. page P. verreauxi Propithecus verreauxi PCR polymerase chain reaction PCV packed cell volume pp. pages rpm rounds per minute rRNA ribosomal ribonucleic acid s.s-1 substitutions per site SFV simian foamy virus SMS smart model selection sp. species spp. species (plural) ST sequence type TP total protein UDOI utilization distribution overlap index µl mikroliter µM mikromolar XI XII 1. Introduction 1. Introduction Parasitism – an ecological perspective Almost all organisms are affected by parasitism, be it as hosts or as parasites. Throughout this thesis, the term “parasite” will be used according to the ecological definition: “…any organism that lives on and draws nutrients from another organism (the host), usually to the host’s detriment” (Nunn and Altizer 2006). This definition encompasses a wide range of biological diversity in the form of viruses, bacteria, protozoa, fungi, helminths and arthropods. Parasites use their host both as a source of energy and as a habitat in a “prolonged and durable way” (Combes 2001), which gives rise to a system more complex than the sum of its parts. Parasites exhibit considerable morphological simplification and loss of genes while relying on the host to provide them with the corresponding functions (Combes 2001); a parasite is thus often reliant on the host
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