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Conservation of South African Tortoises with Emphasis on Their Apicomplexan Haematozoans, As Well As Biological and Metal-Fingerprinting of Captive Individuals

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Conservation of South African Tortoises with Emphasis on Their Apicomplexan Haematozoans, As Well As Biological and Metal-Fingerprinting of Captive Individuals CONSERVATION OF SOUTH AFRICAN TORTOISES WITH EMPHASIS ON THEIR APICOMPLEXAN HAEMATOZOANS, AS WELL AS BIOLOGICAL AND METAL-FINGERPRINTING OF CAPTIVE INDIVIDUALS By Courtney Antonia Cook THESIS submitted in fulfilment of the requirements for the degree PHILOSOPHIAE DOCTOR (Ph.D.) in ZOOLOGY in the FACULTY OF SCIENCE at the UNIVERSITY OF JOHANNESBURG Supervisor: Prof. N. J. Smit Co-supervisors: Prof. A. J. Davies and Prof. V. Wepener June 2012 “We need another and a wiser and perhaps a more mystical concept of animals. Remote from universal nature, and living by complicated artifice, man in civilization surveys the creature through the glass of his knowledge and sees thereby a feather magnified and the whole image in distortion. We patronize them for their incompleteness, for their tragic fate of having taken form so far below ourselves. And therein we err, and greatly err. For the animal shall not be measured by man. In a world older and more complete than ours they move finished and complete, gifted with extensions of the senses we have lost or never attained, living by voices we shall never hear. They are not brethren, they are not underlings; they are other nations caught with ourselves in the net of life and time, fellow prisoners of the splendour and travail of the earth.” Henry Beston (1928) ABSTRACT South Africa has the highest biodiversity of tortoises in the world with possibly an equivalent diversity of apicomplexan haematozoans, which to date have not been adequately researched. Prior to this study, five apicomplexans had been recorded infecting southern African tortoises, including two haemogregarines, Haemogregarina fitzsimonsi and Haemogregarina parvula, and three haemoproteids, Haemoproteus testudinalis, Haemoproteus balazuci and Haemoproteus sp. A. The taxonomy of all of these species was questionable, and therefore one goal of this study was to examine at least some in great detail with the view to resolving taxonomic issues. This involved using a number of techniques such as light microscopy and image analysis, transmission electron microscopy, and molecular analysis. Outcomes were the transfer of one Haemogregarina species (Haemogregarina fitzsimonsi) to the genus Hepatozoon, the suggestion that the genus Hemolivia might be more appropriate for another haemogregarine (Haemogregarina parvula), the synonymisation of two known species of Haemoproteus (Haemoproteus balazuci with Haemoproteus testudinalis), and the naming of a third haemoproteid (Haemoproteus natalensis Cook, Smit and Davies, 2010). In addition, a likely new species of haemogregarine (Haemogregarina sp. A.) was described. To achieve all this, 367 tortoises were collected representing 62% of the species and all five genera, of South African tortoises. Tortoises were both wild (287) and captive (80), with these being both live (270) and dead (97) when taken. They were located in four different provinces, including Gauteng, KwaZulu-Natal, the Northern and the Western Cape, and in four different biomes (semi-arid grassland, Kalahari desert, subtropical thorn bushveld, and coastal endemic fynbos). Light photomicroscopy examination of Giemsa stained peripheral blood smears prepared from the subcarapacial vessels of live tortoises allowed for descriptions and comparisons of the observed haematozoans. Of the live tortoises, 14.8% had haemogregarines, including 13.3% with H. fitzsimonsi, 0.7% with H. parvula, and 0.7% with a previously unknown, intraleucocytic, Haemogregarina sp. A. A further 1.1% had haemoproteids, including 0.7% with Hp. testudinalis/Hp. balazuci and 0.4% with Haemoproteus sp. A. The host and locality records of previously described haematozoan species were increased and records for likely new species provided. Subtropical areas (KwaZulu-Natal) compared to arid regions (Northern Cape) presented with a higher diversity of apicomplexans, along with a higher prevalence of ticks, possible vectors of the tortoise blood parasites. Overall, male tortoises had the highest haematozoan and tick prevalences compared to females and juveniles, I whilst juveniles showed the highest parasitaemias. Ticks collected from tortoises included Amblyomma marmoreum, Amblyomma sylvaticum, and Ornithodorus compactus. Tick prevalence was high in areas where wild tortoises showed high prevalence with H. fitzsimonsi, while captive tortoises from which ticks had been eradicated, showed low haematozoan prevalence. Infections with Haemogregarina and Haemoproteus species were not concurrent, and H. fitzsimonsi occurred in the absence of all other apicomplexans. However, H. parvula and H. fitzsimonsi were always found concurrently, and Haemogregarina sp. A and H. fitzsimonsi co-existed in 50% of the recorded Haemogregarina sp. A. infections. Ultrastructural examination of gamonts of H. fitzsimonsi and H. parvula differentiated between these species, H. fitzsimonsi resembling species of Haemogregarina and Hepatozoon at this level, and the encased gamonts of H. parvula closely resembling those of species of Hemolivia. Molecular analysis of 18S rDNA sequences extracted from methanol-fixed, Giemsa stained tortoise blood films containing H. fitzsimonsi gamonts, and DNA taken from sporogonic stages in formalin and ethanol fixed H. fitzsimonsi infected tick impression slides and tick viscera, revealed that H. fitzsimonsi likely belonged to the genus Hepatozoon. Such analysis also implicated both Amblyomma species as vectors for this parasite, as well as providing insights into the phylogeny of the ticks themselves. No DNA sequences were obtained for Haemogregarina sp. A., likely due to the low parasitaemias observed in tortoise peripheral blood films. However, based on the apparent lack of dividing stages within blood smears and its intraleucocytic nature, Haemogregarina sp. A. was suggested to be a new species of Hepatozoon. Morphometrics allowed for the synonymisation of Hp. balazuci with the earlier described Hp. testudinalis, and Haemoproteus sp. A. was studied more extensively than previously and described as a new species, Haemoproteus natalensis. Other major goals of the thesis were to assess H. fitzsimonsi as a bio-indicator for tortoise body condition, and as a biological tag. However, the apparent relationships among prevalence, parasitaemia and host body condition in two selected tortoise species, Chersinia angulata and Stigmochelys pardalis, were statistically insignificant. Additionally, prevalence and parasitaemia were apparently higher in tortoises in anthropogenically impacted areas than in those in unimpacted reserve areas, but these differences were again statistically insignificant. Haemogregarina fitzsimonsi was thus rejected as a bio-indicator for future tortoise population ‘health’ assessment. Host- specificity, geographical range, prevalence and parasitaemia of the recorded haematozoans suggested that several might eventually prove useful as biological tags, but with H. fitzsimonsi perhaps requiring further genetic analysis to determine whether different strains II of the parasite occur across distinct host species and different tortoise populations. A final goal of the thesis was to attempt to metal-fingerprint tortoises by site. Of all wild tortoise tissues (bone, scute and nail) collected and analysed by inductively coupled plasma spectrometery, nail provided the best resolution among tortoises from different sites. Nail collection, being non-invasive compared to the sampling of other tissue types, supported the proposal of a nail metal-fingerprint database for the future determination of captive tortoise origin, perhaps allowing their return to the wild and thus aiding South African tortoise conservation. III TABLE OF CONTENTS ABSTRACT I TABLE OF CONTENTS IV LIST OF FIGURES XI LIST OF TABLES XXI CHAPTER 1: INTRODUCTION 1.1 Introduction to the field of study 2 1.2 Hypotheses and aims of the study 7 1.3 Objectives of the study 8 1.4 Outline of the thesis 9 CHAPTER 2: LITERATURE REVIEW 2.1 Biomes of South Africa 13 2.1.1 Influence on tortoise and associated parasite diversity 13 2.2 Characteristics of tortoises 14 2.2.1 General introduction 14 2.2.2 Classification 15 2.2.3 South African genera 16 2.2.4 Tortoise evolution 24 2.2.5 Tortoises as hosts 25 2.3 Blood protozoans of tortoises 26 2.3.1 General introduction 26 2.3.2 Classification 27 2.3.3 Apicomplexan evolution 29 2.3.4 Haematozoans of reptiles 30 IV 2.3.5 Haematozoans of tortoises with focus on South African genera 30 2.3.6 Molecular analysis of reptile haematozoans with focus on those infecting tortoises 37 2.4 Haematophagous, metazoan ectoparasites of tortoises 38 2.4.1 General introduction to ticks 39 2.4.2 Classification 41 2.4.3 South African genera infecting tortoises 42 2.4.4 Tick evolution 48 2.4.5 Ticks as vectors 49 2.4.5.1 Hyalomma aegyptium, vector for Hemolivia mauritanica (Sergent and Sergent, 1904) Landau and Paperna, 1997 (Apicomplexa: Haemogregarinidae) 50 2.5 Conservation of tortoises with use of bio-indicators, biological tagging and metal-fingerprinting 53 2.5.1 Bio-indicators 53 2.5.1.1 Haemogregarina fitzsimonsi as a bio-indicator 53 2.5.2 Biological tagging and metal-fingerprinting 55 CHAPTER 3: MATERIALS AND METHODS 3.1 Collection sites 59 3.1.1 Wild tortoise collection sites 59 3.1.2 Captive tortoise collection sites 62 3.2 Collection and identification of tortoises 63 3.3 Blood collection for apicomplexan haematozoans infecting tortoises 68 3.4 Examination of tortoise blood 68 3.4.1 Light microscopy 68 3.4.2 Transmission electron microscopy 68 V 3.4.3 Apicomplexan
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