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Influence of Parasites on Fitness Parameters of the European Hedgehog (Erinaceus Europaeus)

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Influence of Parasites on Fitness Parameters of the European Hedgehog (Erinaceus Europaeus) Influence of parasites on fitness parameters of the European hedgehog (Erinaceus europaeus ) Zur Erlangung des akademischen Grades eines DOKTORS DER NATURWISSENSCHAFTEN (Dr. rer. nat.) Fakultät für Chemie und Biowissenschaften Karlsruher Institut für Technologie (KIT) – Universitätsbereich vorgelegte DISSERTATION von Miriam Pamina Pfäffle aus Heilbronn Dekan: Prof. Dr. Stefan Bräse Referent: Prof. Dr. Horst Taraschewski Korreferent: Prof. Dr. Agustin Estrada-Peña Tag der mündlichen Prüfung: 19.10.2010 For my mother and my sister – the strongest influences in my life “Nose-to-nose with a hedgehog, you get a chance to look into its eyes and glimpse a spark of truly wildlife.” (H UGH WARWICK , 2008) „Madame Michel besitzt die Eleganz des Igels: außen mit Stacheln gepanzert, eine echte Festung, aber ich ahne vage, dass sie innen auf genauso einfache Art raffiniert ist wie die Igel, diese kleinen Tiere, die nur scheinbar träge, entschieden ungesellig und schrecklich elegant sind.“ (M URIEL BARBERY , 2008) Index of contents Index of contents ABSTRACT 13 ZUSAMMENFASSUNG 15 I. INTRODUCTION 17 1. Parasitism 17 2. The European hedgehog ( Erinaceus europaeus LINNAEUS 1758) 19 2.1 Taxonomy and distribution 19 2.2 Ecology 22 2.3 Hedgehog populations 25 2.4 Parasites of the hedgehog 27 2.4.1 Ectoparasites 27 2.4.2 Endoparasites 32 3. Study aims 39 II. MATERIALS , ANIMALS AND METHODS 41 1. The experimental hedgehog population 41 1.1 Hedgehogs 41 1.2 Ticks 43 1.3 Blood sampling 43 1.4 Blood parameters 45 1.5 Regeneration 47 1.6 Climate parameters 47 2. Hedgehog dissections 48 2.1 Hedgehog samples 48 2.2 Biometrical data 48 2.3 Organs 49 2.4 Parasites 50 3. Statistics 51 III. THE EXPERIMENTAL HEDGEHOG POPULATION 52 1. Results 52 1.1 Tick population 52 1.1.1 Larvae 55 1.1.2 Nymphs 56 1.1.3 Females 57 1.1.4 Males 58 5 Index of contents 1.1.5 Ticks and climate parameters 59 1.2 The hedgehog population 62 1.3 Hedgehog weight 64 1.3.1 Annual weight distribution 64 1.3.2 Hedgehog weight and ticks 67 1.4 Cortisol 68 1.4.1 Annual cortisol levels 68 1.4.2 Cortisol and tick infestation 71 1.4.3 Cortisol and climate parameters 72 1.5 Testosterone 76 1.5.1 Annual testosterone levels 76 1.5.2 Testosterone and tick infestation 78 1.5.3 Testosterone and cortisol 79 1.5.4 Testosterone and climate parameters 80 1.6 Haematological values 83 1.6.1 Haematological values and tick infestation 85 1.6.2 Haematological values and climate parameters 92 1.7 Regeneration 95 1.7.1 Comparison of the R- and C-groups 95 1.7.2 Comparison of sampling dates within the R-group and the C-group 99 2. Discussion 103 2.1 Haematological values, ticks and climate parameters 103 2.2 Tick population dynamics and regulation 105 2.2.1 Sex-biased tick infestation 105 2.2.2 Tick population dynamics and regulation 107 2.3 Cortisol 112 2.4 Testosterone 117 2.4.1 Annual testosterone levels 117 2.4.2 Testosterone and tick infestation 118 2.5 Haematological values and regeneration 120 2.5.1 Blood count 120 2.5.2 Regeneration 124 2.5.3 Consequences of tick-induced blood loss 125 3. Summary 129 6 Index of contents IV. HEDGEHOG DISSECTIONS 132 1. Results 132 1.1 Parasite distribution 132 1.1.1 Germany 132 1.1.2 UK 137 1.1.3 New Zealand 140 1.1.4 Comparison of the investigation areas 147 1.2 Parasites and fitness related parameters 159 1.2.1 Condition factor 159 1.2.2 Organs 164 1.2.3 Sexual Organs 170 2. Discussion 177 2.1 Parasite distribution 177 2.2 Comparison of investigation areas 183 2.3 Parasites and organs 184 2.4 Parasites and host reproduction 192 3. Summary 193 V. CONCLUSIONS AND PERSPECTIVES 196 VI. REFERENCES 198 ACKNOWLEDGEMENTS 233 APPENDIX I 235 APPENDIX II 236 APPENDIX III 245 APPENDIX IV 248 APPENDIX V 252 APPENDIX VI 254 7 Index of figures Index of figures Figure 1: Natural distribution of Erinaceus europaeus and E. amurensis . 21 Figure 2: Natural distribution of Erinaceus roumanicus and E. concolor . 21 Figure 3: Overview of the muscles of a hedgehog. 22 Figure 4: Method of nest construction by a European hedgehog. 23 Figure 5: Female and male hedgehog fleas ( Archaeopsylla erinacei ). 28 Figure 6: Caparinia tripilis from skin samples of a European hedgehog. 29 Figure 7: Larvae of Trombicula autumnalis on a European hedgehog. 30 Figure 8: Tick species infecting Erinaceus europaeus . 31 Figure 9: Developmental cycle of Crenosoma striatum . 32 Figure 10: Section of an opened lung from a European hedgehog. 33 Figure 11: View on the eastern part of the hedgehog garden. 42 Figure 12: Person securing an unrolled hedgehog. 44 Figure 13: Hind leg of a hedgehog with a placed tourniquet. 44 Figure 14: Multivette tube inserted in the saphenous vein of a hedgehog. 45 Figure 15: Primary sex characteristics of hedgehogs. 49 Figure 16: Illustration of the reproductive organs of hedgehogs. 50 Figure 17: Seasonal distribution of mean larval tick numbers. 55 Figure 18: Seasonal distribution of mean nymph tick numbers. 56 Figure 19: Seasonal distribution of mean female tick numbers. 57 Figure 20: Seasonal distribution of mean male tick numbers. 58 Figure 21: Seasonal distribution of mean hedgehog weight. 65 Figure 22: Seasonal distribution of mean hedgehog weight gain (or loss). 66 Figure 23: Annual distribution for mean cortisol levels. 68 Figure 24: Annual distribution for mean testosterone levels. 76 Figure 25: Annual distribution for mean testosterone levels, years pooled. 78 Figure 26: Relationship between erythrocytes and total tick weight. 87 Figure 27: Relationship between haemoglobin and total tick weight. 87 Figure 28: Relationship between haematocrit and total tick weight. 88 Figure 29: Relationship between MCV and total tick weight. 88 Figure 30: Relationship between MCH and total tick weight. 89 Figure 31: Relationship between MCHC and total tick weight. 89 Figure 32: Relationship between relative reticulocyte concentration and total tick weight. 90 Figure 33: Relationship between absolute reticulocyte concentration and total tick weight. 90 8 Index of figures Figure 34: Relationship between lymphocytes and total tick weight. 91 Figure 35: Relationship between neutrophils and total tick weight. 91 Figure 36: Relationship between thrombocytes and total tick weight. 92 Figure 37: Distribution of fleas in the investigation areas. 147 Figure 38: Distribution of Crenosoma striatum in the investigation areas. 148 Figure 39: Distribution of Capillaria aerophila in the investigation areas. 149 Figure 40: Distribution of intestinal Capillaria spp. in the investigation areas. 150 Figure 41: Distribution of trematodes in the investigation areas. 151 Figure 42: Distribution of peritoneal Plagiorhynchus in the investigation areas. 153 Figure 43: Distribution of intestinal Plagiorhynchus in the investigation areas. 154 Figure 44: Distribution of all Plagiorhynchus in the investigation area. 155 Figure 45: Species richness for the different investigation areas. 156 Figure 46: Species richness for age groups in the different investigation areas. 157 Figure 47: Distribution of total tick weight in the investigation areas. 158 Figure 48: Distribution of Ixodes ricinus weight in the investigation areas. 158 Figure 49: Distribution of Ixodes hexagonus weight in the investigation areas. 159 Figure 50: Relationship between body weight and body length of juvenile hedgehogs from Germany. 161 Figure 51: Relationship between body weight and body length of juvenile hedgehogs from the UK. 162 Figure 52: Relationship between body weight and body length of adult hedgehogs from New Zealand. 163 Figure 53: Relationship between body weight and body length of juvenile hedgehogs from New Zealand. 164 9 Index of tables Index of tables Table 1: Bacteria occurring in the European hedgehog. 37 Table 2: Viruses, protozoans and fungi occurring in the European hedgehog. 38 Table 3: Number of hedgehogs used for tick counts. 52 Table 4: Mean numbers of I. ricinus counted during the investigation period. 53 Table 5: Mean numbers of I. hexagonus counted during the investigation period. 54 Table 6: Correlation between temperature and tick density. 60 Table 7: Correlation between relative humidity and tick density. 61 Table 8: Correlation between rainfall and tick density. 62 Table 9: Mortality in the experimental hedgehog population. 63 Table 10: Homogenous subgroups for mean body weight of hedgehogs. 65 Table 11: Homogenous subgroups for mean weight gain (or loss) of hedgehogs. 66 Table 12: Correlation between tick weight and hedgehog weight or weight change. 67 Table 13: Homogenous subgroups for annual cortisol levels of female hedgehogs. 69 Table 14: Homogenous subgroups for annual cortisol levels of male hedgehogs. 70 Table 15: Correlation between tick weight and cortisol levels of female hedgehogs. 71 Table 16: Correlation between tick weight and cortisol levels of male hedgehogs. 71 Table 17: Correlation between temperature and cortisol levels. 73 Table 18: Correlation between relative humidity and cortisol levels. 74 Table 19: Correlation between rainfall and cortisol levels. 75 Table 20: Monthly comparison of mean testosterone levels for 2007 and 2008. 77 Table 21: Monthly comparison of mean testosterone levels for 2006-2008. 77 Table 22: Correlation between tick weight and testosterone levels. 79 Table 23: Correlation between testosterone and cortisol levels. 80 Table 24: Correlation between temperature and testosterone levels. 81 Table 25: Correlation between relative humidity and testosterone levels. 82 Table 26: Correlation between rainfall and testosterone levels. 83 Table 27: Descriptive statistics of the haematological values for 2007 and 2008. 84 Table 28: Means of haematological values from the experimental hedgehog population, QUILLIAM et al. (1971), WENZEL et al. (1977) and LEWIS et al. (2002). 85 Table 29: Correlation between tick weight and haematological values for 2007.
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