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This Thesis Has Been Submitted in Fulfilment of the Requirements for a Postgraduate Degree (E.G This thesis has been submitted in fulfilment of the requirements for a postgraduate degree (e.g. PhD, MPhil, DClinPsychol) at the University of Edinburgh. Please note the following terms and conditions of use: This work is protected by copyright and other intellectual property rights, which are retained by the thesis author, unless otherwise stated. A copy can be downloaded for personal non-commercial research or study, without prior permission or charge. This thesis cannot be reproduced or quoted extensively from without first obtaining permission in writing from the author. The content must not be changed in any way or sold commercially in any format or medium without the formal permission of the author. When referring to this work, full bibliographic details including the author, title, awarding institution and date of the thesis must be given. Epidemiology and Control of cattle ticks and tick-borne infections in Central Nigeria Vincenzo Lorusso Submitted in fulfilment of the requirements of the degree of Doctor of Philosophy The University of Edinburgh 2014 Ph.D. – The University of Edinburgh – 2014 Cattle ticks and tick-borne infections, Central Nigeria 2014 Declaration I declare that the research described within this thesis is my own work and that this thesis is my own composition and I certify that it has never been submitted for any other degree or professional qualification. Vincenzo Lorusso Edinburgh 2014 Ph.D. – The University of Edinburgh – 2014 i Cattle ticks and tick -borne infections, Central Nigeria 2014 Abstract Cattle ticks and tick-borne infections (TBIs) undermine cattle health and productivity in the whole of sub-Saharan Africa (SSA) including Nigeria. In this West African country, two thirds of the cattle population are reared in the central- northern regions, kept under the traditional pastoral husbandry of Fulani herders. Under the Fulanis’ management, cattle are grazed extensively, being exposed to infestation by several tick genera (i.e. Amblyomma , Hyalomma , and Rhipicephalus spp., sub-genus Boophilus spp. included), vectors of the causative agents of the most important bovine TBIs in West Africa: anaplasmosis, babesiosis and ehrlichiosis (cowdriosis). Nevertheless, the Fulani pastoralists do not usually employ chemicals to control ticks in their cattle, merely relying on traditional methods (i.e. manual removal of the most conspicuous specimens). This approach, however, does not prevent cattle from being re-infested, leaving the animals challenged by a broad variety of other tick species, most of which are vectors of economically relevant TBIs. Knowledge of tick and TBIs occurrence is an essential pre-requisite to assist field diagnosis and devising effective control strategies for a given area. Existing information on tick infestation of cattle in Nigeria is rather out-dated, mostly derived from studies carried out in the south of the country. Similarly, all studies published to date on cattle TBIs in the country do not include any molecular analysis, being based instead on cytological and/or serological diagnostics. Therefore, the aim of the present thesis was to assess the presence of cattle ticks and TBIs occurring in an area of Central Nigeria (i.e. Plateau State). This is a densely populated area with traditionally managed cattle, where no acarides have historically been employed on livestock. The work undertaken herein firstly reviews the information available to date on ticks and TBIs known to be endemic in Nigerian cattle, identifying gaps present in the existing knowledge, leading to the rationale of this study. An initial survey was conducted documenting the tick species infesting cattle in Central Nigeria, in ii Cattle ticks and tick -borne infections, Central Nigeria 2014 order to assess the infestation rate of surveyed animals at the time of the year when the tick load on the host is known to be most abundant (i.e. the wet season). The survey provided novel information on tick populations in cattle in Nigeria disclosing the presence of a broad variety of species, most of which are vectors of hazardous TBIs. In order to conduct a molecular diagnosis of the TBIs within the study area, a novel methodology was developed (i.e. reverse line blotting, RLB). The application of this approach was based on a thorough review of its application to the diagnosis of TBIs worldwide as well as in SSA. The optimisation of the RLB at the University of Edinburgh to enable the detection of a broad-spectrum of TBIs in Nigeria, caused by an array of five genera of microorganisms (i.e. Ehrlichia and Anaplasma , Theileria and Babesia , Rickettsia spp.) is presented. The assessment of the analytical sensitivity of this technique for the detection of Anaplasma marginale , a highly endemic tick-borne pathogen in SSA, demonstrated a detection threshold of ≥ 7 infected cells (keeping the limit of a natural infection). The occurrence of TBIs in cattle in the study area was assessed during a large-scale epidemiological survey through the application of the validated RLB. This study disclosed the occurrence of a high prevalence of several bovine TBIs in Central Nigeria, some of which are of great veterinary and zoonotic concern. The RLB enabled the detection of carrier status as well as of numerous multiple infections (69.5%, 95% CI: 65.5–73.6%). Based on the findings presented, endemic stability for highly prevalent haemoparasites (i.e. Theileria mutans , Theileria velifera , Theileria taurotragi , Anaplasma marginale , Ehrlichia species Omatjenne) is postulated, whereas a more instable epidemiological scenario is hypothesized for other microorganisms (i.e. Anaplasma centrale and Babesia bovis ), which might be connected with outbreaks of clinically apparent disease, sporadically seen in the study area. The effect of a monthly tsetse-borne trypanosomiasis-focused control programme (based on the application 0.005% deltamethrin spray formulation, iii Cattle ticks and tick -borne infections, Central Nigeria 2014 applied only to the lower quarters of cattle) on the kinetics of bovine TBIs was assessed at the village level. Longitudinal monitoring of control and treated cattle was conducted over the period of eleven months. Results generated provide input to the improvement of future control strategies to be rolled out across SSA, aiming to achieve an integrated control of both trypanosomiasis and TBIs. The present thesis contributes to a better understanding of the epidemiology of bovine TBIs in Nigeria as well as in the rest of West Africa, using a highly sensitive tool of wide applicability. These findings will be shared with the local pastoralist communities to further promote effective yet sustainable, vector control, in tune with the traditional long-established practices. iv Cattle ticks and tick -borne infections, Central Nigeria 2014 Table of Contents Abstract ........................................................................................................ ii List of Figures .............................................................................................. x List of Tables ............................................................................................. xiv List of abbreviations ................................................................................. xvii Acknowledgements .................................................................................... xix Chapter 1 – Introduction and Literature Review ................................................... 1 1.1 Introducing the research focus ............................................................... 2 1.2 Literature review .................................................................................... 6 1.2.1 Ticks (Acari: Ixodida) ...................................................................... 6 1.2.1.4 Cattle ticks in SSA ...................................................................... 16 1.2.1.5 Cattle ticks in Nigeria ................................................................. 16 1.2.1.5.1 Amblyomma variegatum (Fabricius, 1794) .............................. 17 1.2.1.5.2 Hyalomma spp. ........................................................................ 19 1.2.1.5.3 Rhipicephalus (Boophilus ) spp. ............................................... 21 1.2.2 Cattle tick-borne infections (TBIs) in SSA.................................... 28 1.2.3 Endemic (enzootic) stability .......................................................... 39 1.2.4 Tick control .................................................................................... 43 1.2.5 The Fulani pastoralist system ........................................................ 56 1.2.6 Tick control on the Nigerian Plateau ............................................. 59 1.3 Thesis aims ........................................................................................... 61 Chapter 2 – Ixodid ticks of traditionally managed cattle in Central Nigeria ..... 63 2.1 Introduction .......................................................................................... 64 2.2 Aims ...................................................................................................... 64 2.3 Materials and Methods ......................................................................... 65 2.3.1 Plateau State ................................................................................... 65 2.3.2 Study area ...................................................................................... 66 2.3.2 Tick sampling and identification
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