The influence of human settlements on gastrointestinal helminths of wild monkey populations in their natural habitat Zur Erlangung des akademischen Grades eines DOKTORS DER NATURWISSENSCHAFTEN (Dr. rer. nat.) Fakultät für Chemie und Biowissenschaften Karlsruher Institut für Technologie (KIT) – Universitätsbereich genehmigte DISSERTATION von Dipl. Biol. Alexandra Mücke geboren in Germersheim Dekan: Prof. Dr. Martin Bastmeyer Referent: Prof. Dr. Horst F. Taraschewski 1. Korreferent: Prof. Dr. Eckhard W. Heymann 2. Korreferent: Prof. Dr. Doris Wedlich Tag der mündlichen Prüfung: 16.12.2011 To Maya Index of Contents I Index of Contents Index of Tables ..............................................................................................III Index of Figures............................................................................................. IV Abstract .......................................................................................................... VI Zusammenfassung........................................................................................VII Introduction ......................................................................................................1 1.1 Why study primate parasites?...................................................................................2 1.2 Objectives of the study and thesis outline ................................................................4 Literature Review.............................................................................................7 2.1 Parasites and host ecology .........................................................................................8 2.1.1 Terminology .........................................................................................................9 2.1.2 Parasites and their role in population regulation ...........................................11 2.2 Disease and wildlife conservation............................................................................14 2.2.1 Disease in the human-wildlife interface ...........................................................16 2.2.2 Cross-transmission between humans and primates .......................................18 2.3 Primates, Protozoa and Macroparasites ................................................................22 2.3.1 Protozoa ..............................................................................................................23 2.3.2 Helminths ...........................................................................................................24 2.3.3 Cross-transmission of macroparasites .............................................................27 Materials and Methods..................................................................................29 3.1 Non-invasive study....................................................................................................30 3.2. Sampling regime ......................................................................................................31 3.3. Laboratory methods................................................................................................33 3.3.1 Sedimentation procedure and microscopic examination ...............................33 3.3.2 Coproculture ......................................................................................................36 3.4 Estimation of intensity of infection by fecal egg counts ........................................37 3.5 Behavioral observations...........................................................................................39 3.6 Statistical analyses ....................................................................................................40 Peru ...........................................................................................................42 4.1 Introduction ..............................................................................................................43 Index of Contents II 4.2 Materials and Methods ............................................................................................44 4.2.1 Study animals .....................................................................................................44 4.2.2 Study area ...........................................................................................................46 4.2.3 Study groups ......................................................................................................47 4.2.4 Study period and sample collection .................................................................49 4.3 Results........................................................................................................................50 4.3.1 Human fecal samples .........................................................................................50 4.3.2 Tamarin fecal samples ......................................................................................54 4.4 Discussion ..................................................................................................................71 4.4.1 Human fecal samples .........................................................................................71 4.4.2 Tamarin fecal samples ......................................................................................73 Thailand .........................................................................................................89 5.1 Introduction ..............................................................................................................90 5.2 Materials and Methods ............................................................................................91 5.2.1 Study animals .....................................................................................................91 5.2.2 Study area ...........................................................................................................94 5.2.3 Study groups ......................................................................................................95 5.2.4 Study period and sample collection .................................................................99 5.2.5 Behavioral data collection ...............................................................................100 5.3 Results......................................................................................................................101 5.4 Discussion ................................................................................................................131 5.4.1 Human fecal samples...........................................................................................131 5.4.2 Macaque samples.................................................................................................135 General Discussion .......................................................................................148 6.1 Disease risk and anthropogenic influence ............................................................150 6.2 Parasites and their impact on the host’s survival................................................154 6.3 Seasonality of the results........................................................................................157 6.4 Directions for further research .............................................................................158 References .....................................................................................................160 Acknowledgments.........................................................................................210 Appendices ....................................................................................................211 Curriculum vitae ..........................................................................................227 Index of Tables III Index of Tables Table 3.1 Description of activity categories applied in the “instantaneous scan sampling”. ........................ 40 Table 4.1 Tamarin study group composition. ................................................................................................... 47 Table 4.2 Composition of gender and age classes of sampled humans from Diamante. ............................... 47 Table 4.3 Human parasite identification. .......................................................................................................... 52 Table 4.4 Descriptive statistics of length and width for eggs of four parasite morphospecies from male and female villagers from Diamante................................................................................................................ 53 Table 4.5 Intensity of infection in human stool samples from Diamante........................................................ 53 Table 4.6 Tamarin parasite identification......................................................................................................... 56 Table 4.7 Descriptive statistics of length and width for eggs of six parasite morphospecies found in tamarins. ..................................................................................................................................................... 57 Table 4.8 Effects of host species and host group on PSR (ANOVA)............................................................... 59 Table 4.9 P-values of Fisher’s exact test comparing prevalence of parasite infection in tamarins.. ............ 63 Table 4.10 Fecal egg and larvae output in tamarin groups.............................................................................. 65 Table 4.11 Mann Whitney