Evolutionary history of the critically endangered giant sable antelope (Hippotragus niger variani). Insights into its phylogeography, population genetics, demography and conservation

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“Black among black shadows” Gilbert Blaine, 1922

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Foreword

In compliance with the no. 2 of article 4 of the General Regulation of Third Cycles of the University of Porto and with article 31 of the Decree-Law no. 74/2006, of 24 March, with the alteration introduced by the Decree-Law no. 230/2009, of 14 September, the results of already published work were totally used and included in some of the chapters of this dissertation. As these studies were performed in collaboration with other authors, the candidate clarifies that, in all these works, participated in obtaining, interpreting, analysing and discussing the results, as well as in the writing of the published forms.

This thesis should be cited as:

Vaz Pinto P (2018) Evolutionary history of the critically endangered giant sable antelope (Hippotragus niger variani). Insights into its phylogeography, population genetics, demography and conservation. PhD Thesis, University of Porto, Porto, Portugal.

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Aknowledgements

This dissertation is a milestone on a long, yet unfinished, journey that I have initiated many years back in the wonderful Angolan bush, and it would not have been possible without a vast array of contributions from many friends. I will try my best to recognize here at least some of the most relevant contributors.

First and foremost to my supervisor Nuno Ferrand, for his brilliance, friendship and enthusiasm while guiding me through this enterprise, and also by adding new layers to my views of the natural world. But most of all because he came up with the idea and convinced me to do the PhD, so quite literally, this work could never have materialized without Nuno.

To my co-supervisor Raquel Godinho, for her guidance, patience and warm hospitality. She forced me to raise my standards, and her pragmatic and hard-working attitude was inspirational and proved crucial for the success of this work. To my informal co-supervisor Pedro Beja for sharing his knowledge and adding several key contributions in critical stages.

I must address special thanks to Luis Veríssimo, with whom I have shared so many brainstorms that provided answers to outstanding questions and new lines of research. And Luis has always been available, donated some of his free time, and ended up kindly producing the majority of maps presented in this work. Also to Joana Rocha for spearheading many tasks in several papers, and to Hugo Fernandes for his artwork. Thank you, to my good friend Filippo Nardin, who has always been there for me and provided critical assistance at various stages of this work.

To my friend Vladimir Russo, for his cool head and by putting down numerous “fires”. To Sendi Baptista for being a wonderful companion and precious collaborator in so many bush trips. To Abias Huongo, for his friendship and precious assistance.

A very special thank you to generals João Traguedo and Afonso Hanga for their friendship, unrelentless continuing support to my work and to the giant sable conservation, and commitment to the cause.

I must also aknowledge my many other Angolan friends who were instrumental in different ways for the success of various stages related to the conservation project on the ground, starting with Kalunga Lima who I have deerly missed, Henriette Koning,

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Wolfram and Werner Brock, Nito Rocha, Harold Roberts, João Sousa, Miguel Morais, Carlos Cunha, David Schaad and Kostadin Louchanski. They were always supportive. The team of local shepherds and rangers in Cangandala and Luando played a decisive role on the ground throughout the project, and several have become friends. A special thanks is due to Manuel Sacaia, for his enthusiasm and good humour, with whom I hope to share many more camp fires in the wilderness under Angolan starry nights.

To Brian Huntley, Richard Estes, Jeremy Andersen and John Walker, for being inspirational and for having shared with me their passion and immense knowledge on the giant sable antelope. And I am hugely indebted to Peter Morkel for his incredible skills and professionalism, and for his truthful and unrestricted commitment to conservation. It has been a privilege to know all of you.

To all the staff at CIBIO, particularly at the lab in CTM, making the magic of transforming tiny biological samples into quantifiable data.

A special mention is due to Carina Matos, Dario Martins, Valdemar Pinto and rest of the staff at Kissama Foundation for their continuing support for many years.

To the Catholic University of Angola and all my good friends at CEIC.

To the Ministry of Environment and Provincial Government of Malanje for having authorized the various research lines, and to all the good people in these institutions that have supported the activities. And of course to the various branches of FAA, the Angolan military forces, in particular the air force, for the outstanding efforts that made possible some of the more challenging initiatives.

I must also express my sincere gratitude to the institutions that have contributed financially to various components of the project, namely Sonangol, Esso Angola, Angola LNG, Whitley Award, Tusk Trust, Fondation Segré. In Particular, Laurentino Silva, Bill Cummings, Fernando Pegado, Miguel Cordeiro, David Mallon have never doubted the value of the project from the onset and ensured continuation of support when needed. The financial donations received from the ExxonMobil Foundation specifically addressed several of the research lines covered by this thesis, and proved to be a critical contribution to the end result.

Finally but not least to my dearest, to my recently deceased father for having exposed me to the bush and wildlife while I was still a little kid, and to my mother for having always been tolerant and supportive. And of course to my lovely wife Paula, and our wonderful kids Beatriz, Afonso, Margarida and Frederico. I hope this work will make them all proud.

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Summary

The African continent is renowned for a remarkable diversity of bovid taxa, the end product of an explosive taxonomic radiation that was sparked by environmental changes during the Miocene. Having adapted to the vast array of ecological niches present in Africa, extant members of this highly speciose family come in many forms and sizes, but arguably none is as rare, revered and poorly known as the giant sable antelope (Hippotragus niger variani), which occupies the centre stage of this dissertation. Described as late as in the early twentieth century, the giant sable has never been found outside a small region confined to the Kwanza River basin in central Angola, and in spite of carrying a high cultural and iconic value, it is also one of the most endangered mammals in the world. Because of its rarity, historical background and the recent political turmoil that affected the country, few studies have focused on this taxon and conservation has been neglected, these constituting critical shortfalls that the current thesis aims to address. On a wider level, the sable antelope could be seen as a model species for biogeographical studies in Africa because it is one of the most highly specialized antelopes, closely associated with particular habitats, and yet widely distributed across the continent. In addition, the economic interest on sable has boomed in recent years, becoming one of the most prized high value species for the fast-growing multi-million dollar game farming industry in Southern Africa. Despite its importance and the increasing attention received by researchers over the years, we have identified various gaps on the species knowledge. Recent studies have relied on mitochondrial DNA fragments and limited datasets to infer phylogeographic patterns and intraspecific taxonomy, yet the results may not have improved much on previous data published by zoologists before the advent of DNA and based on morphological analyses. By adopting new tools and expanding the sampling effort, we expect this dissertation will much improve current knowledge on the species.

Within this framework we started by targeting the conservation crisis facing the giant sable antelope in Angola. The use of new molecular tools, namely autosomal markers not yet available for Hippotragus was considered crucial, and by developing a panel of 57 species-specific microsatellites, also successfully tested on congeneric roan antelope H. equinus, we were able to address specific questions affecting the giant sable, and provide for the first time estimates of genetic diversity further interpreted within the context of other populations. These initial efforts evidenced the giant sable as being seriously depleted of genetic diversity when compared to other sable populations. In

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addition, analyses of allele frequency spectrums and allele sharing between populations, proved to be consistent with an evolutionary history of giant sable characterized by population bottlenecks and long-standing isolation.

A more decisive application for these nuclear markers consisted in providing support to specific conservation initiatives already unfolding on the ground. Here we report on how the sustained use of extensive field research methods based on field, aerial and trap-camera surveys, combined with modern molecular tools, has uncovered and allowed the documentation in unprecedented detail, of a remarkable case of interspecific introgressive hybridization between giant sable and roan antelope in Cangandala National Park. We explore how hybridization was sustained for several years following a steep poaching-induced population crash that led to the extirpation of all giant sable bulls in Cangandala. By demonstrating and quantifying the extent of the phenomenon we illustrate how the lack of conspecific mates can function as a mechanism promoting hybridization and increasing the extinction risk to endangered populations. Concrete actions were also implemented to reverse the extinction vortex in Cangandala, and we document the management measures adopted, including the use of breeding enclosures, veterinarian intervention on the hybrids, chemical immobilization of animals, and translocations, which have ultimately promoted the giant sable recovery in the park. In order to expand the focus of this work we used next-generation sequencing methods to capture complete mitochondrial sequences, and an extensive sampling effort allowed us to obtain hundreds of extant sable samples pooled from across the whole species range. The dataset was further enhanced by adding important historical samples that filled a few geographical gaps and provided us with highly informative temporal sequences. With these tools available we investigated sable phylogeographic patterns in much greater detail and resolution than had previously been possible, and were able to clarify outstanding questions. The existence of a highly divergent mitochondrial lineage in west Tanzania was reinterpreted as signature of a past introgressive event involving an extinct taxon, and in addition we identified three main lineages in sable that originated nine haplogroups. These haplogroups are remarkably clustered into six geographical groupings well delimitated by physical boundaries. Our findings are consistent with an evolutionary history of the species shaped by Pleistocene climatic oscillations, but also highlights the role of geomorphological barriers such as rifts, rivers and mountain chains. In particular we hypothesize that late Pleistocene rearrangements in the Zambezi drainage system may help explain some vicarance episodes inferred to have occurred in southern Africa. Surprisingly, the giant sable antelope was found to be part of a central African lineage, sharing a common maternal ancestry with sables

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currently present in Malawi and west Tanzania, and therefore we suggest that the lineage may have originated in the Congo basin.

Applying the panel of microsatellites on our dataset resulted in the first comprehensive population genetics study of H. niger. Our results confirmed that contemporary sable populations display strong structuring patterns induced by physical barriers and demographic processes. We were able to define five main and well-defined population clusters, largely concordant with results obtained with mitogenomes except for the region of east Zambia and Malawi where recent mitochondrial introgression is suggested. Patterns of differentiation observed are indicative of low levels of gene flow among the main clusters, but contact zones were identified in east Zambia and central Mozambique. These results point towards the discrimination of five taxa for an intraspecific taxonomy, strongly supporting the validity of H. n. niger, H. n. roosevelti, H. n. kirkii and H. n. variani, and suggesting that the west Tanzanian sable may in the future warrant subspecific status.

We have successfully extracted DNA and tested the famous and mysterious Florence horn, which proved to be the earliest known material ascribed to giant sable, and predating the subspecies description in over forty years. By amplifying mitogenomic sequences from other historical giant sable samples obtained in museums and private collections in Europe and America, we have quantified a relevant loss of diversity resulting from a recent bottleneck. Two main mitochondrial lineages were identified in giant sable, but one of them, represented in the Florence horn and a few other historical samples, survived at least until 1982 and yet appears now to be extinct. These findings underline how the use of modern molecular tools can enhance natural history collections, and stress the value of these collections to inform and assist in the conservation of endangered populations.

Globally, we believe that this dissertation makes a significant contribution to address the plight of the giant sable, by unveiling the evolutionary processes that shaped the natural history of this magnificent antelope, and by assisting the implementation of specific conservation measures on the ground and developing new and still ongoing lines of research. At species level, this work constitutes a major improvement on previous knowledge regarding evolutionary relationships, phylogeographic patterning, degrees of differentiation and gene flow, and intraspecific taxonomy. Interpreting these results on a wider scale may provide important insights to explain general patterns of vicariance and speciation, and inter-relationships among closely related populations that ultimately may help us to better understand the biogeography of the African continent.

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Resumo

O continente Africano é conhecido pela sua notável diversidade de bovídeos, o produto final de uma radiação taxonómica explosiva que foi desencadeada por transformações ambientais durante o Mioceno. Tendo-se adaptado a uma vasta diversidade de nichos ecológicos existentes em África, os atuais membros desta especiosa família surgem em várias formas e tamanhos, mas possivelmente nenhum é tão raro, admirado e pouco conhecido como a palanca-negra-gigante (Hippotragus niger variani), espécie que desempenha o papel principal nesta dissertação. Descrita apenas no início do século XX, a palanca-negra-gigante ocorre apenas numa pequena região confinada à bacia do Rio Kwanza, no coração de Angola, e apesar de manter um elevado valor cultural e simbólico, é também um dos mamíferos mais ameaçados de extinção no mundo. Por causa da sua raridade, antecedentes históricos e recente agitação política que afetou o país, poucos estudos se focaram neste táxon e a sua conservação foi igualmente negligenciada, pelo que a presente tese pretende atenuar estas importantes limitações. Numa escala mais alargada, a palanca-negra pode ser vista como uma espécie modelo para estudos de biogeografia em África não apenas por ser um dos antílopes mais especializados, fortemente associado a habitats específicos, mas também pela sua extensa distribuição no continente. Adicionalmente, o interesse económico das palancas teve um grande incremento em anos recentes, ao tornar-se uma das espécies mais valiosas e procuradas pela milionária indústria das fazendas de caça na África Austral. Apesar da sua importância e da crescente atenção recebida por investigadores ao longo dos anos, foram identificadas várias falhas no conhecimento da espécie. Estudos recentes recorreram a fragmentos de DNA mitocondrial, mas os resultados podem não ter melhorado muito os publicados em trabalhos anteriores pela zoologia tradicional e baseados em análises morfológicas. Adotando novas ferramentas e expandindo o esforço de amostragem, espera-se que esta dissertação venha a constituir uma importante contribuição para o conhecimento da espécie.

Neste enquadramento começou-se por lidar com a crise de conservação enfrentada pela palanca-negra-gigante em Angola. O uso das novas ferramentas moleculares, nomeadamente marcadores autossómicos até então não disponíveis para os Hippotragus, foi considerado essencial, e através do desenvolvimento de um painel de 57 microsatélotes específicos para a espécie, também testados com sucesso na congenérica palanca-ruana H. equinus, tornou-se possível abordar questões

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específicas que afectavam a palanca negra gigante, fornecendo pela primeira vez estimativas da sua diversidade genética e enquadradas no contexto de outras populações. Adicionalmente, análises dos espectros de frequências alélicas e partilha de alelos entre populações, revelaram-se consistentes com uma história evolutiva da palanca negra gigante caracterizada por estrangulamentos populacionais e isolamento geográfico prolongado.

Uma aplicação mais decisiva destes marcadores nucleares consistiu no auxílio a iniciativas de conservação específicas que já estavam a decorrer no terreno. Aqui reporta-se como o uso extensivo de métodos de campo baseados em levantamentos terrestres, aéreos e com recurso a câmaras ocultas, combinado com modernas técnicas moleculares, revelou e permitiu a documentação com um detalhe sem precedentes, de um notável caso de hibridação e introgressão interespecífica entre a palanca-negra-gigante e a palanca-ruana no Parque Nacional da Cangandala. Explora-se aqui como a hibridação se manteve por vários anos no seguimento de um colapso populacional severo causado por caça-furtiva e que levou ao desaparecimento de todos os machos reprodutores na Cangandala. Ao ser demonstrada e quantificada a extensão do fenómeno, ilustra-se como a ausência de reprodutores conspecíficos pode funcionar como um mecanismo promotor de hibridação e desta forma aumentar o risco de extinção de populações ameaçadas. Foram também adoptadas ações concretas, incluindo a construção de recintos para reprodução, intervenção veterinária nos híbridos, imobilização química de animais e translocações, que em última análise promoveram a recuperação das palancas-negras-gigantes no Parque Nacional.

De forma a expandir o âmbito deste trabalho foram utilizados métodos de sequenciação de nova-geração, e um amplo esforço de amostragem que nos permitiu obter centenas de amostras atuais de palancas provenientes de quase toda a sua área de distribuição. O conjunto de dados foi ainda reforçado adicionando importantes amostras históricas que preencheram algumas falhas geográficas e constituiram sequências temporais muito informativas. Com estas ferramentas disponíveis, foram investigados padrões de filogeografia na palanca com muito mais detalhe e maior resolução do que foi possível até aqui, clarificando-se desta forma questões pendentes. A existência de uma linhagem mitocondrial altamente divergente na Tanzânia ocidental foi reinterpretada como uma assinatura de um evento passado de introgressão envolvendo um táxon extinto, e permitiu ainda a identificação de três linhagens principais na palanca que deram origem a nove haplogrupos. Estes haplogrupos agruparam-se de forma notável em seis regiões geográficas bem delimitadas por barreiras físicas. Estes resultados são consistentes com uma história evolutiva da espécie moldada por oscilações climáticas do

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Pleistoceno, mas também realçam o papel de barreiras geomorfológicas tais como rifts, rios e cadeias montanhosas. Em particular, é avançada como hipótese que rearranjos no sistema de drenagem do Zambeze no final do Pleistoceno podem ajudar a explicar alguns dos episódios de isolamento que se infere terem ocorrido na África Austral. Surpreendentemente, os dados mostraram que a palanca-negra-gigante é parte da linhagem central, partilhando um ancestral comum com palancas atualmente presentes no Malawi e Tanzânia ocidental, e assim sugerimos que esta linhagem pode ter tido origem na bacia do Congo.

A aplicação do painel de microsatellites ao conjunto de dados resultou no primeiro estudo abrangente de genética populacional em H. niger. Os resultados obtidos confirmaram que as populações de palanca-negra contemporâneas evidenciam fortes padrões de estruturação induzidos por barreiras físicas e processos demográficos. Foi possível definir cinco populações principais e bem-delineadas, largamente concordantes com os resultados obtidos com a mito-genómica excepto para a região do Malawi e Zâmbia oriental, onde uma introgressão mitocondrial recente é sugerida. Os padrões de diferenciação observados são indicativos de reduzidos valores de fluxo génico entre os principais agrupamentos populacionais, mas zonas de contacto foram identificadas na Zâmbia oriental e no centro de Moçambique. Estes resultados sugerem a discriminação de cinco taxa para uma taxonomia intraespecífica, dando forte suporte para a validade de H. n. niger, H. n. roosevelti, H. n. kirkii e H. n. variani, e sugerindo ainda que as palancas da Tanzânia ocidental poderão no futuro merecer estatuto subespecífico.

Foi extraído e testado com sucesso ADN do famoso e misterioso corno de Florença, que demonstrou ser o mais antigo material conhecido atribuído à palanca-negra-gigante, antecipando a descrição da subespécie em mais de quarenta anos. Através da amplificação de sequências mito-genómicas de outras amostras históricas de palanca-negra-gigante obtidas em museus e coleções privadas na Europa e América, foi possível quantificar uma relevante perda de diversidade genética resultantes de um estrangulamento populacional recente. Duas linhagens mitocondriais principais foram identificadas na palanca-negra-gigante, sendo que uma delas, representada no corno de Florença e nalgumas outras amostras históricas, sobreviveu pelo menos até 1982 mas parece estar agora extinta. Estes resultados sublinham como o uso de modernas ferramentas moleculares podem enriquecer as coleções de história natural, e reforçam o valor destas colecções para informar e auxiliar na conservação de populações ameaçadas.

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Globalmente, acreditamos que esta dissertação fornece uma contribuição decisiva para lidar com a situação dramática em que se encontra a palanca-negra-gigante, revelando os processos evolutivos que moldaram a história natural deste magnífico antílope, e ajudando na implementação de medidas específicas de conservação no terreno e no desenvolvimento de novas linhas de investigação e de outras ainda em curso. A nível da espécie, este trabalho constitui um avanço significativo em termos de conhecimento disponível relativamente às relações evolutivas, padrões filogeográficos, graus de diferenciação e fluxo génico, e taxonomia intraespecífica. A interpretação destes resultados a uma escala mais alargada pode providenciar importantes contribuições para explicar padrões gerais de isolamento e especiação, e inter-relações entre populações evolutivamente próximas, que em última análise podem ajudar a compreender melhor a biogeografia do continente Africano.

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Keywords

Ancient DNA, Angola, antelope, bottleneck, conservation genetics, demography, giant sable, hybridization, Hippotragus equinus, Hippotragus niger variani, introgression, microsatellites, mtDNA, nuclear markers, phylogeography, population genetics

Palavras-chave

Angola, antílope, demografia, DNA antigo, efeito de gargalo, filogeografia, genética da conservação, genética populacional, hibridação, Hippotragus equinus, Hippotragus niger variani, introgressão, marcadores nucleares, microsatélites, mtDNA, palanca-negra-gigante

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List of Tables and Figures

CHAPTER 1 – General Introduction

Fig. 1.1 – Giant sable bull in Luando Nature Reserve 3

Fig. 1.2 – Typical sable skull compared with giant sable skull 4

Fig. 1.3 – Sizes of sable trophy horns in Rowland Ward’s record book 5

Fig. 1.4 – The Florence horn and museum label 6

Fig. 1.5 – Sable head drawing from original description 7

Fig. 1.6 – Photos of hunting trips in Angola, (a) Anita Curtis with bull

shot, and (b) Count of Yebes with world trophy record 9

Fig. 1.7 – Researchers monitoring the giant sable in the 1970s 10

Fig. 1.8 – Map with location of the giant sable reserves in Angola 12

Fig. 1.9 – Images depicting habitat, (a) aerial view of woodlands in

Luando, and (b) anhara covered with geoxyle vegetation 13

Fig. 1.10 – Feeding sequences, (a) bull browsing on leaves, and

(b) herd with calves browsing on geoxyles 14

Fig. 1.11 – Aerial view of giant sable herd in Luando 15

Fig. 1.12 – Giant sable herd recorded by trap camera in Cangandala NP 19 Fig. 1.13 – Hybrids sableXroan, (a) Female hybrid from Kruger NP, and

(b) hybrids recorded with trap camera in Cangandala NP 21

Fig. 1.14 – Cladogram representing phylogenetic relationships among

extant Hippotragini 22

Fig. 1.15 – Plate depicting head of extinct bluebuck 25

Fig. 1.16 – Drawings representing heads of roan and giant sable 26

Fig. 1.17 – Maps showing the main phytocorias of the African savanna

biome and ecoregions, superimposed on the distributions of

(a) Roan, and (b) sable 30

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Fig. 1.19 – Cladograms representing intraspecific phylogenies adapted

from previous efforts, for (a) roan, and (b) sable 39

CHAPTER 2 – Consequences of a population collapse

Paper I

Table 1 – Genetic diversity measures for three populations of H. niger

and one sample of H. equinus, based on microsatellites 67

Fig. 1 – Allele frequency spectrum obtained from 57 and 54 microsatellites

for three H. niger populations and one H. equinus sample 68 Supplementary Information

Table S1 – Genebank accession number, primer sequences, repeat motif

dye, and multiplex conditions of 57 msats for H. niger 73

Table S2 – Genetic diversity measures by locus for three populations of

H. niger and for H. equinus, based on microsatellites 77

Table S3 – Loci with Linkage Desiquilibrium 79

Paper II

Fig. 1 – Distribution of sable and roan in Africa, and study area 83

Fig. 2 – Temporal variation in population size and births of giant sable

and hybrids in Cangandala NP 90

Fig. 3 – Schematic representation of diagnostic field characteristics of

giant sable, roan, hybrids and backcrosses in CNP 91

Fig. 4 – Genetic evidence for sable X roan hybridization in CNP, with (a)

first and second components of a principal component analyses, and (b) individual assignment to genetic clusters inferred by

Bayesian analyses, with program Structure 92 Supplementary Information

Fig. S1 – Photos obtained from camera trapping in the study area 101

Fig. S2 – Different stages of the giant sable translocation program 102

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Table S2 – Genetic diversity measures for populations of H. niger

and for H. equinus, based on 51 microsatellites 103

Table S3 – Inferred ancestry of sableXroan hybrids in Cangandala NP 104

CHAPTER 3 – Sable phylogeographic patterns and population structuring

Paper III

Fig. 1 – Distribution range of H. niger and origin of samples 114

Fig. 2 – Neighbor-Net network based on uncorrected patristic distances

in SplitsTree excluding sites with insertions/ deletions 115

Table 1 – Genetic diversity summary statistics based on complete

mtDNA genome sequences 116

Fig. 3 – Medium-joining networks based on complete mtDNA sequences

for each of the different geographic genetic groups 117

Table 2 – Median time for the most recent common ancestor and 95%

Highest posterior density intervals 118

Fig. 4 – Evolutionary history of sable lineages across the species range

and in relation to geographical features in Africa 121 Supplementary Information

Table S1 – List of modern samples with country and population 140

Table S2 – List of historic samples with age, country and population 148

Table S3 – Priors used for Bayesian analyses of divergence times 149

Table S4 – Genetic distances between different H. niger lineages 150

Table S5 – Genetic diversity summary statistics and standard deviations

based on complete mtDNA genomes 150

Table S6 – Genetic diversity summary statistics and standard deviations

for the highly divergent mtDNA sequences in Tanzania 151

Fig. S1 – Bayesian phylogenetic tree for 215 H. niger and 2 H. equinus

based on whole mitochondrial genomes 152

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Paper IV

Fig. 1 – Population structure in pie charts and sable sample locations 162

Fig. 2 – Population substructure in pie charts for the main groups found

in SplitsTree excluding sites with insertions/ deletions 163

Table 1 – Measures of genetic diversity by main groups and subgroups 164 Fig. 3 – Scatterplot of the first two principal components of DAPC

evidencing the five genetic clusters considered 166

Fig. 4 – Scatterplot of the first two principal components of DAPC

for nine subgroups, excluding Angolan and Tanzanian sable 167

Fig. 5 – Cavalli-Sforza network based on 50 microsatellites, showing

the genetic subdivision in 12 subgroups 168

Table 2 – Genetic differentiation (Pairwise Fst) among the main groups 168 Table 3 – Hierarchical analyses of molecular variance (AMOVA)

examining the partinioning of genetic variation 169 Supplementary Information

Table S1 – Geographic origin, group assignment and sample size 188

Table S2 – Hardy-Weinberg calculations performed with ARLEQUIN 190

Table S3 – List of localities and average likelihood (Qi) of individual

assignment by origin to the five main clusters 191

Table S4 – Genetic differentiation (Pairwise Fst) among 12 subgroups 193 Table S5 – Results for the Mantel Test to determine isolation by distance

within the five main sable groups 193

Fig. S1 – (a) Posterior likelihood values (LK) and (b) ΔK, for 10

independent Structure runs for the whole dataset 193

independent Structure runs for the Southern population 194

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independent Structure runs for the Zambian population 194

independent Structure runs for the West Tanzanian population 195

independent Structure runs for the Angolan population 195

CHAPTER 4 – The giant sable in natural history collections

Paper V

Fig. 1 – (a) The Florence horn, and (b) aerial photo of a giant sable bull 201 Table 1 – List of contemporary samples with origin and subspecies 203

Table 2 – List of historical samples with age, origin and subspecies 204

Fig. 2 – Maximum likelihood tree for the Florence horn and 32 sables

based on whole mitochondrial genomes 205

CHAPTER 5 – General Discussion

Fig. 5.1 – Schematic representation of mitochondria capture

following hybridization and introgression 215

Fig. 5.2 – Schematic representation of mitochondrial diversification

within sable based on whole mitochondrial genomes 218

Fig. 5.3 – Sable distribution and clustering based on (a) mtDNA, and

(b) microsatellites 219

Fig. 5.4 – Reconstruction of southern hemisphere palaeoclimates 222

Fig. 5.5 – Main African geomorphological features that have influenced

sable diversification and current distribution 225

Fig. 5.6 – Distribution of major 5 sable populations and 12 subpopulations

in relation to major geophysical features 228

Fig. 5.7 – Graphic representation proposed and traditional taxonomy, in

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Fig. 5.8 – Giant sable areas overlaying detailed maps of (a) soils, and

(a) tree cover and vegetation 236

Fig. 5.9 – Images of sable X roan hybrid backcrosses 241

Fig. 5.10 – Recent demography of sables and hybrids in CNP 242

Fig. 5.11 – Current and historical range of giant sable and haplotype

network, based on whole mitochondrial genomes 245

Fig. 5.12 – Core areas of historical distribution of giant sable in LNSR 247

Table 5.1 – Measures of genetic diversity in giant sable, comparing

nuclear and mtDNA, CNP and LNSR, recent and historical 248

Fig. 5.13 – Accessing giant sable historical material: (a) museum skulls

(b) sample extraction from old trophy 252

Fig. 5.14 – Plate depicting giant sable translocations, collaring and

handling an injured animal 255

Fig. 5.15 – Age pyramids comparing current and theoretical populations 256

Fig. 5.16 – Giant sable spatial use inferred from GPS collars 257

Fig. 5.17 – Graphic representation of average bi-weekly movements of

male and females, with data compiled from GPS collars 258 Appendix I

Fig. Ap.1 – Giant sable areas overlaying maps of (a) average rainfall

and (b) tree cover and temperature 284

Fig. Ap.2 – Giant sable areas overlaying maps of (a) river basins

and (b) hill-shaded relief 285

Fig. Ap. 3 – Giant sable areas overlaying distribution of landforms 286

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Abbreviations

AD: anno Domini

AFS: Allele Frequency Spectrum

AMWE: Angolan Miombo Woodlands Ecoregion AR: Allelic Richness

a.s.l.: at surface level bp: base pair

C4: Carbon 4

CNP: Cangandala National Park

DAPC: Discriminant Analyses of Principal Components DNA: Deoxyribonucliec Acid

DRC: Democratic Republic of Congo EAM: Eastern Arc Mountains

EARS: Eastern African Rift System FAD: First Appearance Date FIS: inbreeding coefficient

FST: fixation index

GIS: Geographic Information System GLD: Genotypic Linkage Desiquilibrium GPS: Global Positioning System

HE: expected heterozygosity

HO: observed heterozygosity

HPDI: Highest Posterior Density Interval HVR: Hypervariable Regions

HW: Hardy-Weinberg

HWE: Hardy-Weinberg Equilibrium IBD: Isolation By Distance

IUCN: International Union for the Conservation of Nature kya: thousand years ago

LIG: Last Interglacial

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MCMC: Monte Carlo Markov Chain MCP: Minimum Convex Polygon MIS: Marine Isotopic Stage mtDNA: Mitochondrial DNA mya: million years ago NA: Number of Alleles

NGS: Next-Generation Sequencing NHC: Natural History Collections NP: National Park

NPA: Number of Private Alleles nuDNA: nuclear DNA

PCA: Polymerase Chain Reaction PCA: Principal Component Analyses SCI: Scientific Citation Index

SR: Strict Reserve

TMRCA: Time for the Most Recent Common Ancestor

UNITA: União Nacional para a Independência Total de Angola WWF: World Wildlife Fund

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CHAPTER 1

GENERAL INTRODUCTION

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1.1 The giant sable antelope

The term antelope evolved from the Byzantine Greek word antholops, referring to a fabulous, elusive and very savage swift beast described by the Bishop of Antioch (AD c336) with saw-shaped horns capable of cutting down trees, that once haunted the banks of the Euphrates (Cuvier and Griffith 1832). Although this legend was likely inspired by earlier observations of the Arabian oryx (Oryx leucoryx), it is hard to ignore how befitting it would be if applied instead to another hippotragine, the giant sable antelope of Angola (Hippotragus niger variani) (Fig. 1.1). Arguably no other antelope than the giant sable has been so praised for its beauty and has sparked so much passion among naturalists, and yet remained framed by mystery and local myth, while becoming one of the most endangered mammals on earth.

Fig. 1.1 – A giant sable antelope bull, photographed in July 2013 from helicopter in Luando Nature Strict Reserve (Photo by author, 2013).

1.1.1 General description

The giant sable is one of four to five generally recognized subspecies of sable antelope (Ansell 1972; Estes 2013). It is a large heavily-built antelope with very long and strongly annulated horns, and narrow pointed ears (Blaine 1922). In giant sable the sexual dimorphism is exaggerated, with large-sized males displaying pitch black glossy coat and contrasting white underparts, while carrying remarkably long and powerful horns

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(Fig. 1.1, 1.2); females on the other hand are smaller, golden to chocolate-brown coloured and have shorter relatively straighter horns (Blaine 1922; Estes & Estes 1974). Giant sable are characterized by a long narrow foreface, and diagnostic dark facial mask lacking a white muzzle stripe to connect the pre-orbital white patch with the also white upper lip (Blaine 1922; Groves & Grubb 2011). The dark face is present in all adult giant sable bulls, but a more or less faint white line is not uncommon in giant sable females or in juvenile males (pers. obs.). Conversely, dark faces have also been occasionally recorded in bulls from populations in west Zambia (Ansell 1974) and west Tanzania.

Fig. 1.2 - Typical sable skull totally contained under a giant sable skull for comparison (Photo by F. Varian, 1953).

The most spectacular feature however is the horn development in giant sable bulls, which grow on average around 30cm longer than in any other known population (Blaine 1922; Walker 2002) (Fig. 1.2). Most typical sable horns from trophies rarely surpass 50 inches as measured along the curvature, but in giant sable they are consistently above that mark and often score over 60 inches (Fig. 1.3). The giant sable horns are strongly compressed laterally and grow perpendicularly to the frontals before curving backwards, crowning a comparatively long skull sustained by a massive, oval in section, and wedge-shaped neck (Blaine 1922). The very long spiralling horns and muscular build observed in bulls much contribute to a perceived “gigantism” of this population, even if there remaine conflicting views on how much larger they are when compared with other sable (e.g. Blaine 1922; Estes 2013).

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Fig. 1.3 - Sizes of sable trophy horns as measured in inches along the main curvature, listed in the Rowland Ward’s Book of Records of Big Game (Halse 1998). The trophies were assigned to three groups, the eastern corresponding to sable from Kenya and northeastern Tanzania (N=12), the royal or giant sable corresponding to Hippotragus niger variani (N=52), and all remaining sable referred here as typical sable (N=1135). To be eligible as record, typical and giant sable had minimum thresholds of 42 and 56 inches respectively. The symbols above the chart represent the average and standard deviation for each group.

1.1.2 Discovery, hunting and the onset of conservation

The story of the giant sable’s exposure to the western world can tentatively be traced back to forty years before its formal scientific description. In 1873 one single, 61 inch-long curved horn of unknown provenance was added to the zoological collection of “La Specola” in Florence1_{. Interestingly, one of the most famous hunters and explorers of its} time, Frederick Selous, visited the museum of Florence and was taken aback by this remarkable horn (Walker 2002) (Fig. 1.4). Perceptively he concluded that not only had to be a sable horn, but because it was so much larger than any other he had ever seen or heard of, this meant that somewhere in southern Africa existed a yet undiscovered and extraordinary breed of grand sable antelope (Walker 2002). Selous became obsessed by the quest for these sables for the rest of his life, but could not solve the horn-mystery.

1_{An even older specimen with 51 inch horns was collected in Angola between 1853 and 1861 by Friedrich Welwitsch} and sent to Lisbon where it was classified by Bocage as Hippotragus niger (Thomas 1916). Unfortunately the specimen was lost in the 1978 fire that destroyed the Museu Bocage, and was never compared with giant sable material.

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Fig. 1.4 – The Florence horn, at the time tentatively ascribed to Hippotragus niger and the label referring the contributions from Frederick Selous in 1894 (Photo by P. Agnelli, 2010).

Instead, the scientific discovery followed the efforts of Mr. Frank Varian, a British engineer who was in Angola in the early twentieth century overseeing the construction of the Benguela railroad (Varian 1953; Walker 2002). In 1909 Varian came across with witness reports and photographs of a remarkably large sable trophy obtained in the Kwanza district, and a couple years later he saw and measured an equally impressive specimen shot by a missionary, but when he reported these observations in letters published in an English journal he was ridiculed by sceptics (Walker 2002). Few would believe that such a remarkable large ungulate could still be unknown in Africa, when even the okapi had been described a decade earlier from the most remote jungle patches of Congo. Undeterred, Varian obtained a series of skins and skulls, also brought from the north of the projected railway route between the Kwanza and Luando rivers, a confined region that for over 50 years would remain as the sole site where the sable could be found. But Varian then left to Europe to serve in the First World War, carrying the skins and skulls, which he dropped at the British Museum of Natural History. Much to the surprise of the mammal curator himself, Oldfield Thomas, the material received from Angola proved to be so distinctive that he even considered the possibility of awarding specific status to the giant sable, before proposing a new subspecies named in honour of Frank Varian in 1916, as Hippotragus niger variani THOMAS 1916 (Walker 2002) (Fig. 1.5). Both Varian and Thomas independently suggested that the Kwanza region in central Angola could have been the likely origin for the mysterious horn housed in Florence.

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Fig. 1.5 – Head of giant sable antelope Hippotragus niger variani, adapted from the original description (Thomas 1916).

The news about the discovery of this magnificent novel race of sable antelope sparked much enthusiasm among naturalists and explorers, eager to resume adventurous trips to exotic locations after the end of the First World War. This led to an increase in the demand to obtain specimens, and many famous hunters offered their services to various natural history museums for the privilege of travelling to Angola and collect giant sables (Walker 2002). In the years following the discovery, numerous expeditions were organized and funded by museological institutions and private individuals, with specimens sent to London, Lisbon, Chicago, New York, Boston or Philadelphia, and notable collectors included the names of Gilbert Blaine, J. G. Millais, Col. J. C. B. Statham, J. Diespecker, Arthur Vernay, Major Powell-Cotton, Prentiss Gray, M. Luna de Carvalho, Cor. B. de Mello and Richard Curtis (Fig. 1.6). In the 1920s the giant sable had become one of the most sought after trophies, a sort of ultimate grail for game hunters (Walker 2002). These trophy hunting exercises were responsible for hundreds of animals shot in the following two decades, adding to subsistence harvesting with traps carried out by locals, and the work of Portuguese and Boer meat hunters. The latter in particular were a major cause of concern when commercial hunting parties organized by Boer hunters had already been credited for wiping out big game in other regions of Angola (Varian 1953; Walker 2002; Huntley 2017). Soon after being formally described, already the future of the giant sable seemed bleak. This scenario would be ameliorated during the Second World War, when organized hunting and foreign trips to Angola were forced to a halt. Once again human conflict had come to the rescue of the beasts. But if the giant sable almost miraculously survived into the 40’s a lot of the credit is owed to the very same man whose name was used to christen the giant sable. Frank Varian not only took immense pride on his discovery, but he also assumed a proprietary attitude

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towards the species, becoming a guardian angel of sorts (Walker 2002). Being aware of the uniqueness of the giant sable, he would watch closely the hunting expeditions and often intervene against the bloodlust of famous hunters (Walker 2002). More importantly he took on an advisory role, and on several occasions approached Portuguese colonial administrators alerting them to the plight of the giant sable. In 1913, even before the first specimens had reached Europe but at a time when Varian was already on the trail of the new sables, he became alarmed at the news that a large and ruthless Boer meat-hunting expedition was about to move into the area. Reacting swiftly, Varian appealed to the Colonial Governor of Moxico who accompanied him on a ground visit, and as result a temporary hunting ban was issued for the upper-Kwanza district (Walker 2002). This remarkable decision, even if poorly enforced, may have been one of the first ever conservation measures taken on a Portuguese colony, and aimed at protecting a species that hadn’t even been formally described. Even more decisive was his approach in 1922 to the former governor-general and recently appointed high commissioner for the colony, General José Norton de Matos, in a meeting held in London. Varian then introduced to the commissioner what he claimed to be the rarest and most beautiful animal present in the territory of Angola and made a strong case for its protection. Norton de Matos was sympathetic to Frank Varian’s arguments, and on a visionary decision unheard of in Portuguese colonies, he decreed the giant sable as “royal game” and closed the Kwanza district for shooting and entry, except with a special license to be issued by the corresponding authorities (Walker 2002). Although the ban did not stop well-connected and well-funded hunters to apply for numerous special licenses, it managed to slow down the level of harvesting while preventing completely the Boer incursions. Varian himself credited Norton de Matos’ decision as the one decisive factor that saved the animal from extinction in those early days (Varian 1953). Importantly, it also laid the foundations to elevate the giant sable to its future iconic status.

Of further relevance was the international meeting held in London in 1933 and known as the “Convention Relative to the Preservation of Fauna and Flora in the Natural State”, which resulted in a broad agreement among African colonial powers to protect local animal and plant species, having also been termed as the Magna Carta of wildlife conservation (Boardman 1981). Portugal was one of the signatories and although wouldn’t ratify the convention until 1950, did react earlier by supporting the classification of the giant sable under formal absolute protection (Class A), and by designating a series of game reserves in Angola. It was under this framework that in 1938 was proclaimed the Reserva de Caça do Luando, defining the narrow strip of land confined between the rivers Kwanza and Luando – The Land Between Two Rivers, covering approximately

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8,000 km2_{and designated specifically to protect the species (Huntley 2017). Gradually} the importance of the giant sable was recognized by politicians, and special hunting licenses became rarer and harder to obtain after the Second World War. One notable exception was the Spaniard Count of Yébes who in 1949 was granted a special license to collect two specimens in Luando, including one for the National Museum of Natural Sciences in Madrid, and as result managed to shoot the largest ever sable trophy, measuring 64’’ 7/8 (Halse 1998; Walker 2002) (Fig. 1.6b).

Fig. 1.6 – Results of hunting trips to Angola, (a) Anita Curtis with a freshly killed giant sable bull in 1924, and (b) the Count of Yébes in 1949 with the largest sable trophy ever recorded (Photos in Walker 2004).

New game regulations approved in 1955 and 1957 under the freshly created Conselho de Protecção da Natureza de Angola, not only totally prohibited hunting of giant sable, but also criminalized and set very strict penalties for transgressors, including effective jail time adding to a fine worth of 100,000 escudos (Frade 1958, Frade & Sieiro 1960). Still in 1957, the Luando Game Reserve was elevated in status to a Nature Integral Reserve, in which even touristic visits would be seriously restricted. The unexpected discovery in the late fifties of an additional, albeit smaller, sable population near Malanje town, led to the creation of Cangandala Nature Reserve in 1962, subsequently elevated to a National Park in 1970. By then the species was well established as a national symbol and well protected, and killing one giant sable was seen as one of the most serious offenses against environment in Portuguese colonial Africa. Nevertheless one last authorized and exceptional hunt for a giant sable took place in 1961 by Dr. Teódulo Agundis, a wealthy and well-connected Mexican hunter who was granted the privilege after a long negotiation at the highest level between Mexico and Portugal (Agundis 1965; A. Moreira pers. comm.).

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1.1.3 Research under colonial rule

Following early morphological approaches (Thomas 1916, Blaine 1922), until the late 1950s the giant sable featured mostly in general studies of Angolan mammals (e.g. Monard 1935; Hill & Carter 1941; Newton da Silva 1958). The step-up of protective measures deriving from the game regulations approved in 1955 and 1957, and the increased interest by Portuguese authorities in stimulating scientific production in Angola, resulted in a series of studies led by Portuguese zoologists specifically addressing the giant sable (Frade 1958; Frade & Sieiro 1960; Crawford-Cabral 1965, 1966, 1969, 1970). Some of these efforts produced the first quantifiable data on the species biology (e.g. Frade & Sieiro 1960; Crawford-Cabral 1965, 1969) and prepared the ground for the year-long study carried out by the well-known American zoologist Richard Estes. Between 1969 and 1970, Richard Estes was based in Luando Nature Strict Reserve (LNSR) and conducted the first intensive study, monitoring several herds during a full annual cycle (Estes & Estes 1974) (Fig. 1.7).

Fig. 1.7 – A Government research vehicle in 1970 in LNSR, while monitoring a giant sable herd, including four young females being herded by a large bull (Photo by R. Estes, 1970).

The work done by Estes & Estes (1974) provided the most comprehensive data available on the biology of the species and set the baseline for all future efforts. Much of what is known today derives directly from their findings. In the early seventies, Brian Huntley the South-African ecologist responsible for the development of Angolan protected areas between 1971 and 1975, also took a natural interest on the giant sable, complementing

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some of the seminal biological studies performed by Frade, Crawford-Cabral and Estes, making specific conservation recommendations and advising on related strategic policies (Huntley 1972, 2017).

1.1.4 Historical distribution and population estimations

The giant sable is only known from Central Angola within the Atlantic-flowing Kwanza river basin. The meandering Luando River, one of the largest and oldest tributaries of the Kwanza, separates the two subpopulations present in LNSR and Cangandala National Park (CNP), and in total the historical distribution range covers around 10,000 km2_{. The LNSR constitutes the core area, being a narrow and depressed strip of land} stretching for over 200 km in length and less than 70 km across at its widest (Estes & Estes 2014). The reserve lays between latitudes 10º S and 12º S, being well delimited by discrete natural boundaries such as the large rivers Kwanza and Luando, and by a series of swamps and cliffs in the southernmost range. CNP is 50 km to the north and much smaller in size covering roughly 630 km2_{, and unlike LNSR, lacking clear natural} boundaries (Fig. 1.8). It is possible that historically, giant sable were more widely distributed in Angola, and witness accounts recorded the presence of animals in the region between the two reserves and even more than one hundred km away into neighbouring provinces, but such claims, often of isolated individuals, remained doubtful or inconclusive (Huntley 1972; Estes & Estes 1974; Crawford-Cabral & Veríssimo 2005). Dispersing males may often reach areas quite distant from the source regions as it has been documented in other sable populations (e.g. Butynski et al. 2016), however these offshoots tend to be exceptional so in practical terms the area defined by the boundaries of CNP and LNSR remain as the home of the giant sable.

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Fig. 1.8 – Location of the two giant sable reserves, Cangandala National Park and Luando Nature Strict Reserve, within the context of Angola.

The remoteness of the region, the rarity and elusive character of the species, the vegetation thickness and the lacking of intensive surveys, prevented reliable censing methodologies, and estimations had to rely on extrapolating figures (Crawford-Cabral 1966, Estes & Estes 1974). Nevertheless, consensus among scientists suggested a total population from the 1950s until early 1970s, between 1,500 and 2,500 animals in LNSR and under a couple hundred in CNP (Crawford-Cabral 1966, 1970; Huntley 1972; Estes & Estes 1974). These numbers correspond roughly to 0.25 sables per km2_{, reflecting the} fact that we’re dealing with a low density and patchily distributed species (Estes & Estes 1974; Estes 2013). The historical numbers of giant sable may have been affected by anthropogenic persecution and habitat destruction, but more likely they had remained rare and sparsely distributed for a much longer period, ecologically constrained as result of very particular habitat requirements (Blaine 1922; Huntley 1972; Estes & Estes 1974).

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1.1.5 Biology

Habitat

In a broader sense and similarly to all remaining sable populations, giant sables are specialists of miombo, a type of woodlands and mesic savannas that grow on poor dystrophic soils and dominated by trees from the genus Brachystegia, Julbernardia and Isoberlinia (Estes 2013). Giant sables are ecotone species, showing a preferential use of the edge between woodland and grassland (Estes & Estes 1974; Estes 2013). One peculiar feature of the giant sable regions is the alternation of more or less thick miombo woodlands in relatively flat or gently undulating terrain (Fig. 1.9a), with vast termite-infested clearings - known by the local name of anharas (Estes & Estes 1974). The anharas are covered by grasslands or fire-prone geoxyle vegetation, the latter consisting of dwarf shrubs also known as underground forests (Barbosa 1970; Huntley 1982; Maurin et al. 2014; Bond 2016; Finckh et al. 2016) (Fig. 1.9b). This mosaic of woodland and different types of anharas seems to constitute the prime habitat for giant sable herds both in LNSR and CNP (Estes & Estes 1974). Giant sables are also a water-dependant species, and the availability of water, in streams or water holes, during the dry season, is a key component determining the habitat value and can become a limiting factor affecting the distribution patterns (Estes & Estes 1974).

Fig. 1.9 – (a) Aerial view of LNSR, showing the Luando River and a mosaic of floodplain, woodlands and grassy anharas (Photo by author, 2004); (b) a detail of an anhara covered by geoxyle vegetation in CNP (Photo by author, 2015).

Food preferences

Giant sables are predominantly grazers (feeding on grasses) but also browse frequently on foliage (Estes & Estes 1974; Estes 2013; pers. obs.). They tend to be selective grazers, favoring palatable perennial grasses such as Brachiaria, Digitaria, Panicum or Setaria spp., and typically biting off only the tender outer portion of the plants (Estes & Estes 1974). The choice of the grass species varies throughout the year depending on

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the vegetation phenology, so that they are harvested at their peak of nutritious value (Estes & Estes 1974). Complementing the grazing, there is little doubt that giant sables also resort often to browsing (Fig. 1.10a). One particularly important shrub is Diplorhynchus condylocarpon, an abundant species in the woodlands of LNSR and CNP, which has been recorded by several authors as a preferential browse all year-round (Statham 1922; Crawford-Cabral 1970; Estes & Estes 1974) (Fig. 1.10a). Other relevant browsing species include the tree Julbernardia paniculata, and the dwarf shrubs Mucana stans, Cryptosepalum maraviense and Dolichus sp (Silva 1972; Estes & Estes 1974) (Fig. 1.10). Geophagy is another feeding behaviour often recorded in giant sable, likely as a mechanism that has evolved in poor soils to extract missing nutrients by eating soil in natural salt licks, usually located in ancient termite mounds (Estes & Estes 1974; Baptista et al. 2013).

Fig. 1.10 – Giant sable feeding sequences in CNP: (a) bull browsing on burnt leaves of Diplorhynchus condylocarpon (Photo by author, 2012); (b) females, juveniles and calves browsing on fresh sprouts of geoxyle dwarf shrubs (Photo by author, 2016).

Social behavior

Giant sables are gregarious and similarly to other social antelopes, display three different social classes, the breeding or nursery herds, bachelor groups and territorial bulls (Estes 2013). The main social unit is the matriarchal herd, composed of breeding cows, respective calves and young (Estes 2013). The total numbers and composition of giant sable breeding herds changes seasonally and sometimes even daily, and different average figures have been obtained ranging from 17 to 24 animals (Crawford-Cabral 1970; Estes & Estes 1974; Estes 2013) (Fig. 1.11). These sedentary nursery herds are led by one of the oldest breeding cows, and tend to perpetuate their home ranges across generations (Estes & Estes 1974; Estes 2013). Young males will be tolerated within the herd until around 3 years of age, when they disperse and may join other stray young males to form bachelor groups (Estes & Estes 1974). These small bachelor groups numbering less than 10 sub-adults, often share their origin from a given nursery herd

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(Estes & Estes 1974). As bulls mature and enter their sixth year of age, they tend to become territorial, patrolling and defending a particular locality, which they will demarcate by scrapping, defecating and bush-thrashing with their horns (Estes & Estes 1974). The same authors report on a complex territorial and dominating system in which younger or sub-dominant bulls may overlap within territories and even get temporary access to breeding herds. Dominant bulls display aggressive behaviour towards intruders, exerting domination by physical intimidation and chasing, and only exceptionally the confrontation leads to a serious fight (Estes & Estes 1974).

Fig. 1.11 – Aerial view in LNSR of a typical giant sable herd in the late dry season, comprising breeding females, juveniles and calves, and accompanied by a territorial bull (Photo by author, 2011).

Breeding

Giant sables are annual seasonal breeders. The rutting generally unfolds during the early rains (pers. obs.), in what can be called as miombo springtime, and Estes & Estes (1974) recorded this behaviour to start in late August. The gestation has been determined for sable antelopes to last for 8.5 to 9 months (Wilson & Hurst 1977), and therefore the calving season for giant sable matches the onset of the dry season, for a two month period between May and July (Estes & Estes 1972). Although the peak of calving is relatively well-defined, a certain number of calves are annually born off-season (Estes & Estes 1974). Females are fertile at two years of age and calve on their third year, and fertility rates are usually very high (Wilson & Hirst 1977; Martin 2003; Estes 2013). As the calving season approaches, the breeding herds tend to break and the most heavily pregnant cows will isolate themselves (Estes & Estes 1974). Giant sables are “hiders”, meaning that females will calve alone and hide their calves, attending them at irregular intervals for several days or weeks, before re-joining the herd with their offspring (Estes

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& Estes 1974; Estes 2013). Calves of similar age will usually stick together within breeding herds forming characteristic crèches (Estes 2013).

Spatial use

Giant sable herds make use of home ranges of varying size, with one of two giant sable herds monitored for one year in Luando reserve staying within 12 km2_{while the other} moved a distance of 15 km to use different areas in the dry and rainy seasons (Estes & Estes 1974). The movement patterns of herds are expected to change according to the annual breeding cycle and seasonal food availability, with the largest concentration of animals observed in the dry season when they congregate to the anharas, to feed on the post-burn flushes (Estes & Estes 1974). With the first rains the larger groups tend to break up, and the herds will leave the anharas and start to focus and feed more often inside the woodlands (Estes & Estes 1974). During the wettest periods, sables will avoid the waterlogged areas such as floodplains, and spend most of the time in high ground within the woodland (Crawford-Cabral 1970, Estes & Estes 1974). The daily movements of herds tend to be modest, typically varying from one to two km (Estes & Estes 1974). In general, herd movement patterns can be summarized as concentrations in open areas during the dry season, followed by group partition as the rain starts and confinement of smaller stable groups in wooded parts of their range, and then increased movements towards the end of the rains and further group fragmentation prior to the calving season (Estes & Estes 1974). Different herds will not overlap in home ranges and are frequently separated by several km of seemingly suitable habitat (Estes & Estes 1974). Sable bulls can hold relatively small territories separated from neighbours by 1-3 km apart, while spending most of their time within 3-4 km2_{but are able expand their area to at least} 10-12 km2_{when accompanying breeding herds (Estes & Estes 1974).}

1.1.6 Cultural significance

The cultural relevance of the giant sable antelope should not be underestimated. Much before it came to be admired worldwide as one of the most impressive and beautiful African mammals, it seems likely that the giant sable already enjoyed some sort of totem status among the resident communities (Walker 2002). Known locally as “Côlô” or “Kolwah” by the Songo and “Sumbakaloko” by the Lwimbi tribes (Statham 1922; Frade e Sieiro 1960), the exact relationships established between the resident communities and their sacred animal are poorly understood but it has been suggested that locals