African Ark: Mammals, landscape and the ecology of a continent 1776147812, 9781776147816

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AFRICAN ARK

AFRICAN ARK Mammals, landscape and the ecology of a continent Ara Monadjem with Mike Unwin

Published in South Africa by: Wits University Press 1 Jan Smuts Avenue Johannesburg 2001 www.witspress.co.za Copyright © Ara Monadjem 2023 Published edition © Wits University Press 2023 Images and figures © Copyright holders All maps and tables by Ara Monadjem unless otherwise indicated First published 2023 http://dx.doi.org.10.18772/12023027809 978-1-77614-780-9 (Paperback) 978-1-77614-781-6 (Hardback) 978-1-77614-782-3 (Web PDF) 978-1-77614-783-0 (EPUB) All rights reserved. No part of this publication may be reproduced, stored in a retrieval system, or transmitted in any form or by any means, electronic, mechanical, photocopying, recording or otherwise, without the written permission of the publisher, except in accordance with the provisions of the Copyright Act, Act 98 of 1978. All images remain the property of the copyright holders. The publishers gratefully acknowledge the publishers, institutions and individuals referenced in captions for the use of images. Every effort has been made to locate the original copyright holders of the images reproduced here; please contact Wits University Press in case of any omissions or errors. This publication is peer reviewed following international best practice standards for academic and scholarly books. Support from the BRO Trust and Oppenheimer Generations Research and Conservation.

Project manager: Elaine Williams Copyeditor: Karen Press Proofreader: Alison Lockhart Indexer: Marlene Burger Cover design: Ayanda Phasha Typeset in 10.5 point Minion Pro

I dedicate this book to Themb’alilahlwa Mahlaba, professor, close friend and colleague, who has taught me more than he realises or than I am willing to acknowledge publicly.

CONTENTS

LIST OF PLATE PHOTOGRAPHS  LIST OF FIGURES AND TABLES  ACKNOWLEDGEMENTS  FOREWORD  PROLOGUE Mammals and Landscapes – the Evolution of a Continent  CHAPTER 1 A Continent of Plenty 

ix xi xix xxi 1 5

CHAPTER 2 The Species Conundrum 

37

CHAPTER 3 The History of Africa’s Mammals 

56

CHAPTER 4 Islands as Species Factories 

79

CHAPTER 5 Evolution on the African Mainland 

99

CHAPTER 6 Giant Mammals Shaping the Landscape 

125

CHAPTER 7 A Place for Every Species 

149

CHAPTER 8 Fluctuating Populations 

170

CHAPTER 9 The Human Factor 

192

CHAPTER 10 The Sinking Ark? 

217

GLOSSARY  NOTES  REFERENCES  RECOMMENDED READING  INDEX 

241 247 257 279 287

LIST OF PLATE PHOTOGRAPHS

1

A collage of African bats. From top left, clockwise: Hypsignatus monstrosus; Rhinolophus hillorum; Macronycteris vittatus; Taphozous mauritianus; Mops leonis; Nycteris arge; Miniopterus nimbae; Scotophilus nux. Photographs by Ara Monadjem. 

2

A brush-furred rat (Lophuromys sikapusi), a beautiful and abundant rodent of the Upper Guinea rainforest zone of west Africa. Photograph by Ara Monadjem. 

3

An arboreal tree rat (Thallomys paedulcus) climbing a bush at Satara Rest Camp in the Kruger National Park, South Africa. Photograph by Mike Unwin. 

4

A bush squirrel (Paraxerus cepapi) in the Kruger National Park, South Africa. Photograph by Ara Monadjem. 

5

A tiny 8-gram shrew (Myosorex meesteri) captured in the Chimanimani Mountains, Mozambique. Photograph by Ara Monadjem. 

6

The highly localised and threatened Nimba otter-shrew (Potamogale lamottei), photographed beside a small stream in the East Nimba Nature Reserve, Liberia. Photograph by Ara Monadjem. 

7

A yellow-spotted rock hyrax (Heterohyrax brucei) in Hwange National Park, Zimbabwe. Photograph by Mike Unwin. 

8

A dwarf mongoose (Helogale parvula) stretching on a fallen trunk in the Kruger National Park. Photograph by Ara Monadjem. 

9

A herd of savanna elephants (Loxodonta africana) in Tsavo National Park, Kenya. Photograph by Ara Monadjem. 

10

A small herd of wildebeest (Connochaetus taurinus) in the Kruger National Park, with a calf standing next to its protective mother. Photograph by Ara Monadjem. 

11

A large herd of zebra (Equus burchelli) and wildebeest (Connochaetes taurinus) in the Maasai Mara National Reserve, Kenya, in 2009. Photograph by Ara Monadjem. 

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x

12

Zebra (Equus burchelli) and wildebeest (Connochaetes taurinus) in Ngorongoro Crater, Ngorongoro Conservation Area, Tanzania. Photograph by Mike Unwin. 

13

A white rhinoceros (Ceratotherium simum) in the Kruger National Park, its horn removed by game rangers in order to stem the tide of poaching. Photograph by Ara Monadjem. 

14

Common chimpanzees (Pan troglodytes) in Kibale National Park, Uganda. Photograph by Mike Unwin. 

15

A cheetah (Acinonyx jubatus) in the Central Kalahari Game Reserve, Botswana. Photograph by Mike Unwin. 

16

A spotted hyena (Crocuta crocuta) waiting below a tree in which a leopard (not visible) is feeding on an impala carcass. Photograph by Ara Monadjem. 

LIST OF FIGURES AND TABLES

FIGURE 1.1

Map of Africa and associated islands. 

FIGURE 1.2

The Southern African vlei rat (Otomys auratus). Photograph by Ara Monadjem. 

10

FIGURE 1.3

Trees pushed over by elephants in the Maasai Mara National Reserve, Kenya. Photograph by Ara Monadjem. 

15

FIGURE 1.4

Kristine Bohmann (left) and Christina Noer (right) testing the telemetry equipment used to track molossid bats in the Simunye region of Eswatini. Photograph by Ara Monadjem. 

17

FIGURE 1.5

An African white-backed vulture (Gyps africanus) in flight in the Maasai Mara National Reserve, Kenya. Photograph by Ara Monadjem. 

20

FIGURE 1.6

Map showing major African ecosystems based on the Terrestrial Ecoregions of the World (Olson et al. 2001). 

23

FIGURE 1.7

Ecosystems discussed in this book. (a) Savanna (Serengeti National Park, Tanzania), (b) forest (Bwindi Impenetrable Forest, Uganda), (c) desert (Namib Desert, Namibia) and (d) mountains (Malolotja Nature Reserve, Eswatini). Photographs by Mike Unwin. 

26

Ecosystems discussed in this book. (a) Aquatic (Zambezi River, Zimbabwe), (b) marine (humpback whale, Megaptera novaeangliae, a regular sight off Africa’s Indian Ocean coast), and (c) fynbos (Blue Hill Nature Reserve, South Africa) (c). Photographs by Mike Unwin (aquatic, marine) and Ara Monadjem (fynbos). 

33

FIGURE 1.8

7

FIGURE 2.1

Mountain gorillas (Gorilla beringei beringei). Photograph by Mike Unwin.  38

FIGURE 2.2

A black spitting cobra (Naja nigricincta woodi). Photograph by Andrew A. Turner. 

41

FIGURE 2.3

The double helix structure of the DNA molecule. Graphic created by Sandile Motsa. 

46

FIGURE 2.4

A Rüppell’s horseshoe bat (Rhinolophus fumigatus) from Mozambique. Photograph by Ara Monadjem. 

48

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FIGURE 2.5

The rough moss frog (Arthroleptella rugosa). Photograph by Andrew A. Turner. 

53

FIGURE 3.1

A Deinotherium. Drawing by Mike Unwin. 

57

FIGURE 3.2

A Lystrosaurus. Drawing by Mike Unwin. 

60

FIGURE 3.3

An Egyptian free-tailed bat (Tadarida aegyptiaca). Photograph by Lindy Lumsden. 

64

FIGURE 3.4

Map of plate tectonics showing the outline of continents over the past several hundred million years (from Pangaea to the present). Drawing by Mike Unwin. 

68

FIGURE 3.5

A yellow-spotted hyrax (Heterohyrax brucei). Photograph by Ara Monadjem. 

71

FIGURE 3.6

Oribi (Ourebia ourebi) in Murchison Falls National Park, Uganda. Photograph by Mike Unwin. 

76

FIGURE 4.1

Map of the western Indian Ocean islands mentioned in this chapter. 

81

FIGURE 4.2

Map of the islands of the Gulf of Guinea and Mount Cameroon. 

87

FIGURE 4.3

A fossa (Cryptoprocta ferox), an example of a euplerid carnivore, the whole family being endemic to Madagascar. Photograph by Ara Monadjem. 

89

FIGURE 4.4

A giant jumping rat (Hypogeomys antimena) at Kirindy Mitea National Park, western Madagascar. Photograph by Ara Monadjem. 

91

FIGURE 4.5

Lemurs: (a) An indri (Indri indri) at Andasibe-Mantadia National Park and (b) a Verreaux’s sifaka (Propithecus verreauxii) at Kirindy Mitea National Park. Photographs by Ara Monadjem. 

94

FIGURE 4.6

Steve Goodman (second left) regaling students on a Tropical Biology Association field course at Kirindy Mitea National Park, western Madagascar, in 2014. Photograph by Ara Monadjem. 

96

A Midas free-tailed bat (Mops midas), a large molossid bat that occurs both in Madagascar and mainland Africa with little genetic differentiation between these populations. The animal was roosting in the roof of a house. Photograph by Ara Monadjem. 

97

FIGURE 4.7

FIGURE 5.1

FIGURE 5.2

xii

(a) Distributions of roan (Hippotragus equinus) and sable (H. niger) antelopes based on information from the IUCN (2019). Grey shading indicates the distribution of roan and grey stippling the distribution of sable. A roan antelope (b) and sable antelope (c), both in Hwange National Park, Zimbabwe. Photographs by Mike Unwin.  Map of the Rift Valley and the Congo Basin. Elevation is shown from light grey (low elevation) to black (high elevation), with the larger rift valley lakes shown in white. The broken white lines show the boundaries of the rift valleys.

101

List of Figures and Tables

The solid black lines show the Congo River and its northern tributary, the Oubangui River. 

103

FIGURE 5.3

A wood mouse (Hylomyscus simus), Sierra Leone. Photograph by Ara Monadjem. 

105

FIGURE 5.4

Mount Nimba, showing the grassy slopes at higher elevations. Photograph by Ara Monadjem. 

108

FIGURE 5.5

Map of the distribution of the two gorilla species Gorilla gorilla (stippled) and G. beringei (grey shading). The Congo and Oubangei rivers are shown as thick black lines, with the Oubangei branching to the north. Note the absence of gorillas in the forested region in between. 

111

FIGURE 5.6

A black-backed jackal (Canis mesomelas), Kruger National Park, South Africa. Photograph by Ara Monadjem. 

114

FIGURE 5.7

Distribution of chimpanzee species in relation to river barriers in west Africa. Note how the large rivers Sanaga, Congo and Oubangui form the borders of the species or subspecies of chimpanzees, attesting to the importance of rivers as barriers to African terrestrial mammals. Pan paniscus is the bonobo, while Pan troglodytes verus, Pan troglodytes ellioti, Pan troglodytes troglodytes and Pan troglodytes schweinfurthii are subspecies of the common chimpanzee Pan troglodytes. 

117

FIGURE 5.8

A west African soft-furred mouse (Praomys rostratus), Sierra Leone. Photograph by Ara Monadjem. 

119

FIGURE 5.9

Peter Taylor removing a rodent (not visible) from a Sherman live trap in northern South Africa. Photograph by Ara Monadjem. 

121

FIGURE 5.10 Map showing location of Mount Elgon in relation to other high

east African mountains. Note the isolated nature of these uplands (shown in darker colours, with black shading indicating areas above 3 200 metres), which gave rise to the ‘islands of the sky’ moniker. 

122

FIGURE 6.1

The four groups of megafauna alive today: (a) elephants, (b) rhinoceroses, (c) hippopotamuses and (d) giraffes. Photographs by Ara Monadjem. 

128

FIGURE 6.2

The number of species of megafauna present in the Late Pleistocene with the number of species remaining today in parentheses. Based on Malhi et al. (2016). 

130

Map of the maximum extent of the ice sheets (grey shaded areas) during the last glacial event (18 000 years ago). Based on Batchelor et al. (2019). 

132

FIGURE 6.4

A giant Aldabra tortoise (Aldabrachelys gigantea). Photograph by Ara Monadjem. 

135

FIGURE 6.5

An acacia tree recently pushed over by elephants in Serengeti National Park, Tanzania. Photograph by Mike Unwin. 

137

FIGURE 6.3

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A channel in the Okavango Delta, bustling with life, thanks to the ecosystem services provided by the hippopotamus (Hippopotamus amphibius). Photograph by Ara Monadjem. 

139

American and Emaswati students collecting ecological data in Hlane Royal National Park, Eswatini. Seated on the left is Charles Gumbi, who was completing a PhD at the University of Florida at the time this photograph was taken, after doing his undergraduate and MSc degrees at the University of Eswatini. Photograph by Ara Monadjem. 

143

FIGURE 6.8

Laurence Kruger demonstrating how one should be doing vegetation analyses: on one’s hands and knees with one’s face close to the ground. Note the fence in the background, a herbivore exclosure camp in Gorongosa National Park, Mozambique, where similar processes are being studied to those described in this book taking place in the Kruger National Park and Eswatini. Photograph by Tara Massad. 

145

FIGURE 6.9

Bob McCleery inspecting an Anabat bat detector in the Kruger National Park with an elephant (Loxodonta africana) in the background. Several of our camera traps have been destroyed by elephants. Photograph by Ara Monadjem. 

146

FIGURE 7.1

Differences in the shape of the wings of bats. Clockwise from top left: the broad and large wings of fruit bats that need to cover long distances to find fruiting trees; shorter and rounder wings needed to manoeuvre through tangled vegetation; the intermediate wing shape useful for exploiting edge habitats; long, narrow wings allowing fast flight in open situations. 

153

A spectrogram (or sonograph) depicting the echolocation call of a bat in graphical form that was recorded near Manzini in Eswatini. Some 11 notes (pulses) can be seen, each a separate call from the same individual. The horizontal axis shows time (each note is separated by milliseconds). The vertical axis shows frequency (or pitch) and it can be seen that each note begins at a higher frequency that drops off to a lower one over time. The frequency, length and shape of such echolocation notes can frequently be used to identify the unseen (freeflying) bat, but in this case could refer to one of several species with similar calls. 

155

FIGURE 7.3

A lion (Panthera leo) feeding on an elephant carcass in Hwange National Park, Zimbabwe. Photograph by Mike Unwin. 

156

FIGURE 7.4

A Villiers’ long-fingered bat (Miniopterus villiersi), Mount Nimba, Liberia. Photograph by Ara Monadjem. 

158

FIGURE 7.5

a–b. A Kirk’s dik-dik (Madoqua kirki) (mass ca.6 kg) and an African buffalo (Syncerus caffer) (mass ca.600 kg) as examples of small and large herbivorous mammals. Photographs by Ara Monadjem. 

161

FIGURE 6.6

FIGURE 6.7

FIGURE 7.2

xiv

List of Figures and Tables

Topi antelopes (Damaliscus lunatus jimela) grazing in the vicinity of the Maasai Mara National Game Reserve, Kenya. Photograph by Ara Monadjem. 

164

A graph showing the differences in diet of two groups of bats based on stable isotope analysis. The horizontal axis shows the values of the carbon isotope while the vertical axis shows the nitrogen values. Each symbol (circle or triangle) shows the diet of a single individual bat. The circles are located to the left of the triangles, indicating that the diet of these bats is mostly from forested environments, compared with grassland environments for the bats represented by triangles. However, in terms of trophic level, the two groups cover similar ranges on the vertical axis. 

167

FIGURE 8.1

A herd of buffalo (Syncerus caffer) showing at most one calf associated with each cow. Photograph by Ara Monadjem. 

172

FIGURE 8.2

A pouched mouse (Saccostomus campestris). Photograph by Ara Monadjem. 

174

FIGURE 8.3

A hypothetical graph showing the contrasting trends of population growth of an r-selected compared with a K-selected mammal. In the case of a K-selected species (stippled line), its population typically increases gradually until it reaches an asymptote, after which it remains relatively stable. In contrast, the population of an r-selected species (solid line) typically rises and drops quickly, and rarely remains stable at any point in time. 

178

FIGURE 8.4

A Natal multimammate mouse (Mastomys natalensis). Photograph by Ara Monadjem. 

179

FIGURE 8.5

An Egyptian slit-faced bat (Nycteris thebaica). This species that gives birth to just one pup per year. Note the very large ears that this bat uses to locate prey moving on the ground by sound. Photograph by Ara Monadjem. 

184

a–b. Blue wildebeest (Connochaetes gnou) in the Maasai Mara National Reserve, Kenya. Photographs by Ara Monadjem. 

188

The roan antelope (Hippotragus equinus) occupies a wide distribution across the African continent (grey shading). However, population sizes (and hence densities) are not uniform across this distribution, with certain regions supporting far larger populations than others. The known populations that harbour 1 000 or more individuals are shown as black circles; note the greater preponderance of large populations in west Africa. Sources: The map is based on the IUCN (2019) distribution map for roan; the location of large populations is taken from Havemann et al. (2016). 

190

FIGURE 7.6

FIGURE 7.7

FIGURE 8.6

FIGURE 8.7

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A herd of sheep feeding in a conservancy adjacent to the Maasai Mara National Game Reserve, Kenya, where they compete with wild herbivores for grazing. Photograph by Ara Monadjem. 

194

FIGURE 9.2

A farmer building a chilli fence to keep elephants out of his fields, Luangwa Valley, Zambia. Photograph by Mike Unwin. 

195

FIGURE 9.3

A typical homestead with an agricultural field in the foreground, Eswatini. Photograph by Ara Monadjem. 

197

FIGURE 9.4

A traditional storage structure for holding harvested maize in Tanzania, with Steve Belmain (right) from the University of Greenwich, UK, who has spearheaded much of the research that I have been involved with pertaining to small-scale farmers and rodents. Nomfundo Dlamini (left) was the ECORAT manager in 2007–2008. Photograph by Ara Monadjem. 

199

FIGURE 9.5

A single-striped grass mouse (Lemniscomys rosalia) visiting a feeding station, Eswatini. Photograph by Annie Loggins. 

203

FIGURE 9.6

An Egyptian slit-faced bat (Nycteris thebaica), feeding on a stinkbug (Nezara), which is a pest of macadamia trees. Photograph © MerlinTuttle.org. 

205

Lourens Swanepoel fitting a yellow mongoose (Cynictis penicillata) with a tracking device (right). Photograph by Wayne Matthews. 

206

FIGURE 9.8

A Meller’s mongoose (Rhynchogale melleri) with three young in agricultural fields in Venda, northern South Africa. Photogaph by Lourens Swanepoel. 

207

FIGURE 9.9

(a) Wanda Markotter (left) dressed in protective gear while extracting viruses from living bats, and Marinda Mortlock (right), a post-doctoral researcher in Markotter’s lab, assisting with the process; the bats were released unharmed after they were sampled. (b) Wanda Markotter removing her mask after a hard morning of sampling. Photographs by Ara Monadjem. 

211

FIGURE 9.1

FIGURE 9.7

FIGURE 9.10 Julie Shapiro conducting bat-related lab work on a field trip to

north-eastern Eswatini. Photograph by Ara Monadjem. 

214

FIGURE 9.11 Fezile Mtsetfwa (left) and Machawe (Maps) Maphalala

entering data during a field trip at Mlawula Nature Reserve, Eswatini. Mtsetfwa was analysing calls of bats recorded by the same Anabat system that Julie Shapiro was using. Photograph by Ara Monadjem. 

215

FIGURE 10.1 The building that once housed the Department of Zoology at the

University of the Witwatersrand, where I studied zoology in the late 1980s. This building now houses the School of Animal, Plant and Environmental Sciences (APES). Photograph by Chevonne Reynolds. 

xvi

218

List of Figures and Tables

FIGURE 10.2 A rural community neighbouring the Gola National Park,

Liberia. This would have been primary rainforest before it was clear-cut to make space for the houses and fields of this village. Photograph by Ara Monadjem. 

220

FIGURE 10.3 The Kalahari is typically flat and open, with few trees to

provide shade or shelter. Springbuck (Antidorcas marsupialis) are well adapted to surviving in this harsh landscape. Photograph by Mike Unwin. 

224

FIGURE 10.4 Map of the Kavango-Zambezi (KAZA) Transfrontier

Conservation Area, showing the main protected areas included in KAZA (main map), and the central position of KAZA in southern Africa (inset map). All the transfrontier conservation areas in the region are shown in grey shading. Note that KAZA cuts across five southern African countries. 

226

FIGURE 10.5 a–b. The Sorris Sorris Conservancy (top), a Namibian

ecotourism venture, where visitors may see a variety of wildlife including plains zebra (bottom). Photographs by Seth Eiseb. 

230

FIGURE 10.6 Map of Eswatini showing the proclaimed protected areas in

the country (dark grey shading): 1) Malolotja Nature Reserve; 2) Hlane Royal National Park; 3) Mlawula Nature Reserve; 4) Mkhaya Game Reserve; 5) Mlilwane Wildlife Sanctuary; and 6) Mantenga Nature Reserve. Also shown (pale grey shading) are other areas of conservation importance but that have not been proclaimed. 

FIGURE 10.7 Ted Reilly, doyen of conservation in Eswatini. Photograph

by Danny Steyn. 

FIGURE 10.8 Themb’a Mahlaba in traditional attire. Photograph courtesy of

Themb’alilahlwa A.M. Mahlaba. 

233 235 238

TABLE 1.1

Numbers of mammalian species, genera, families, and orders (including marine mammals) found in each of the six zoogeographic regions of the world. 

13

TABLE 2.1

The taxonomic ranks used in the classification of organisms, using the examples of African elephant, striped mouse, Egyptian slit-faced bat, and leopard. 

51

Geological eras, periods and epochs as relevant to the story of mammals. The beginning of each era (in millions of years ago – mya) is also given. 

58

TABLE 3.2

Some of the mammalian interchanges between Africa and Eurasia over the past 60 million years. 

74

TABLE 4.1

Islands associated with Africa, their size and distance from the mainland, and number and composition of the bat fauna. 

84

TABLE 3.1

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xviii

TABLE 8.1

Life history traits of some common southern African rodents in the families Muridae and Nesomyidae. 

175

TABLE 9.1

Examples of ecosystem services provided by African mammals. 

202

TABLE 10.1

Predicted declines of African large mammal species in east African parks, showing the extent of each protected area, the number of species that were known to occur in each of them in the 1970s, and the number of species predicted to remain in each area by Soulé and his colleagues (1979). The data are based on two of their models (model 2 and model 3), which have been shown to be the most accurate with respect to the situation in Tanzania (Newmark 1996). 

222

ACKNOWLEDGEMENTS

A

cknowledgments of this kind are virtually impossible to condense into a few paragraphs. From loving parents and caring schoolteachers, to natural history mentors and university lecturers, all the way to my current and past students – all have had a profound effect on my being able to tell the amazing story of Africa’s mammals. However, I’ll do my best to give brief thanks to the most pertinent players. Space does not allow me to list all the many zoologists, botanists and ecologists whose work over the years has provided the foundation for this book. I am indebted to all of them. Although some are world-famous, most are ‘just’ local specialists with a passion for their field of study; what makes them special to me is that I have had the opportunity to spend time in the field with them, allowing me to learn from their vast collective experience. My particular thanks, however, go to those with whom I have worked more closely, and who are acknowledged in the chapters of this book where I discuss their research and our collaborations. There are, of course, many, many other topnotch researchers studying African ecosystems with whom I have not had the pleasure of sharing field time, and I hope that the omission of their names from the pages of the book will not elicit negative views towards this work. My head of department at the University of Eswatini, Themb’alilahlwa Mahlaba, has been supportive of this project from the beginning, granting me as many concessions as possible to reduce, or rearrange, my teaching load at critical periods. I first started thinking about writing this book about a decade ago, but I had other things to deal with at the time and so didn’t have a first draft until five years ago. I then spent several years trying to convince one publisher after the next to take on the book, to no avail. This is where Mike Unwin comes in.

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A professional natural history and travel writer, whom I first met while he was living and working in Eswatini, Mike took my first draft babblings and turned them into the readable text that you see today. Thanks to Roshan Cader of Wits University Press for her dedication in helping us get this book accepted for publication in the first place, and thanks to Karen Press for carefully and craftfully editing the original manuscript. I am also sincerely grateful to Oppenheimer Generations for generous financial support that has made this book more easily available in Africa. Thanks to Duncan MacFadyen for taking care of all the paperwork. Two anonymous reviewers from Wits University Press made many helpful comments and suggestions that significantly improved the original text. My stepmother Negar Ashraf proofread the entire manuscript. I would like to give special thanks to my wife, Sara Padidar, who has assisted with this project in various ways, by reading some of the chapters, helping with the selection of some of the photographs, and discussing some of the concepts presented in the book.

xx

FOREWORD

A

frica is a hugely diverse continent, with a rich and unique assemblage of plants and animals. This exciting book celebrates Africa’s biodiversity, focused on how this diversity has evolved on the continent. The book concentrates on mammals of Africa, providing fascinating facts on how they interact within the African landscape. It investigates how the megafauna shaped the many ecosystems and landscapes through nutrient cycling, landscape modification and interactions between species. Special attention has also been given to small mammals, a group of animals that includes the world’s two most species-rich mammal orders, namely Rodentia (mice, rats, mole rats, springhares, squirrels and porcupines) and Chiroptera (insect- and fruit- or nectar-eating bats), in many cases, some of the least-known mammals. Often with high densities of up to 300 animals per hectare, small mammals are a major component in the diet of carnivores, raptors and reptiles, and in many cases provide ecosystem services such as pollination. The book also investigates the negative impact of certain mammal groups in terms of disease and agricultural pests. The importance of mammals is well documented, as they play a vital role in ecosystem functioning and are in many cases important indicators of habitat integrity. What this book does is profile Africa as the last truly diverse continent left in terms of mammals and their evolution. It also investigates how this incredible diversity has evolved with humans. The role of competition and predation in structuring mammalian communities over time is also investigated, including how different habitats and niches have led to changes in speciation and how different species can coexist in African savannas. African Ark is a visibly fresh approach to the process of how species are created, through independent, evolutionary pathways, when isolated from each other over time. It affords one the opportunity to understand the relationship

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between different organisms and their classification. The book investigates the impact of colonisation events, as well as radiations and speciation, specifically on islands and the mainland. Ara Monadjem delves into the unique details around barriers to movement, which often lead to divergence. Topics such as factors affecting abundance, life strategies and mammal demography are also discussed. This work also profiles the many threats facing Africa’s mammals and provides thoughtful suggestions on how landscapes outside formal conservation areas can be protected across the continent. The existential threat to these mammals is great, as their habitat is increasingly threatened, either directly by human activities such as mining, agriculture, forestry and urbanisation, or through fluctuating temperatures due to climate change. Monadjem’s wonderful book is a welcome addition to the literature of Africa and adds hugely to public awareness of the evolutionary journey of mammals on the continent. Monadjem is a leading mammologist and is highly respected in scientific circles, as well as for his massive contribution to our understanding of mammals across Africa. Apart from academics and ecologists, this book is targeted at any nature enthusiasts, expanding our knowledge and appreciation of life on the African continent. The book is compelling and unique, adding new dimensions to our understanding of species and their ecological function. It is highly informative, and a must-read. I believe it will open a new world to the reader. The future of Africa’s wild areas relies on our understanding of the complexities of nature in all its facets, including its evolutionary past, and African Ark contributes greatly towards this. The author is to be congratulated on producing such a fantastic, informative and refreshing book. Dr Duncan MacFadyen Head: Research and Conservation Oppenheimer Generations 26 January 2022

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PROLOGUE MAMMALS AND LANDSCAPES – THE EVOLUTION OF A CONTINENT

A

book typically begins with a prologue or introduction describing what the book is about. I would like to begin by describing what this book is not about. First, it is not a textbook. Although the contents are based on the works of published scientists, it is – emphatically! – not an exhaustive study. Second, it is not about the plight of Africa’s wilderness and associated wildlife, as vital as such conservation-oriented books may be. Instead, African Ark celebrates Africa’s biological diversity by introducing readers to how this bewildering array of species has arisen. In other words, this is an introductory book about evolution on the African continent. I have assumed that my target audience has had little formal education in biology. However, I have presented the various scientific articles and books that inform this book in a reference list and list of recommended readings, so that those who wish to dig deeper may follow up on selected themes. I should also perhaps mention that I am from Eswatini (formerly Swaziland), and that much of my experience is naturally rooted in this region and thus reflected in the pages of this book. This book does not attempt to cover topics in a standard systematic fashion – starting with microbes, say, then continuing through invertebrates, fishes and so on. Instead, I have carefully selected a variety of themes to illustrate and explain the fascinating processes that have shaped Africa’s landscapes and continue to unfold across them, many before our very eyes. The focus is on mammals, and I make no apology for this: I am, after all, a trained mammologist who has dedicated several decades to the study of these fascinating creatures. It should

1

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be pointed out, however, that when I think ‘mammal’ in the context of this book, I tend to think first of rodents, shrews and bats rather than the likes of elephants, lions and wildebeest. This is not because I value the larger mammals any less, nor because I wish to follow a contrarian pathway, but simply because small mammals make up the bulk of mammalian diversity, with rodents and bats alone accounting for two-thirds of species. Furthermore, our knowledge of small mammals is poor – many are known only by a scientific name and perhaps a single specimen in a natural history museum collection – and I would thus like to redress the balance by giving them greater consideration. I hope that you will find this a refreshing perspective. Another reason for focusing on mammals is that they play important, often vital, roles in African ecosystems. Elephants, hippopotamuses and rhinoceroses are the ultimate environmental engineers, transforming and structuring landscapes on a scale not typically possible for smaller animals. And from a human perspective, mammals really count – for better or worse. Bats, for example, provide us with positive ecosystem services by feeding on pest insects. Rats and mice, by contrast, can destroy harvests, ‘stealing’ from already impoverished subsistence farmers, while both rodents and bats carry some of the most devastating diseases known to humanity. This focus on mammals is not to belittle the contributions to ecosystems of other vertebrates, however, nor to overlook the immense diversity of arthropods and other invertebrates. Where helpful and appropriate, therefore, this book will also draw upon examples from other groups. Why study mammals from Africa? It might help to rephrase this question as follows. What is unique about Africa that makes it a suitable location for studying evolutionary and ecological processes? Other continents cover a larger area, have more bounteous rivers or loftier peaks, and harbour more biological diversity. The answer lies in Africa’s super-sized mammals. This is the only continent to have retained a more-or-less intact community of such ‘megafauna’ as elephants, rhinoceroses, giraffes and hippopotamuses, as well as the large carnivores that prey upon them. Until recently, such giants occurred on every continent. Mastodons (genus Mammut) and mammoths (Mammuthus) roamed the plains of North America and Europe, and their larger cousins in the genus Deinotherium (the largest of which tipped the scales at 17 tons) flourished throughout Eurasia. Giant ground sloths (Megatherium), the size of modern elephants, occurred in South America, while the hippopotamus-sized marsupial 2

Prologue

Diprotodon roamed Australia. Just 20 000 years ago there were 20 species of megafauna weighing more than a ton in South America alone, far outstripping the number in Africa. In fact, there was a greater megafauna diversity in North America (9 species), Eurasia (12 species) and South and South-East Asia (13 species) than in Africa (7 species). The reason Africa stands out today as a bastion of large mammal diversity is thus not because of some unusual feature that makes the continent uniquely favourable to megafauna. Rather, it is because of the total, or near total, extinction of megafauna elsewhere. Africa is not simply the most diverse continent from a large-mammal perspective; it is the only continent with an intact megafauna community. It is thus the only continent where we can truly study ecological interactions and dynamics as they would have been before the sudden and profound flourishing of Homo sapiens over the past 12 000 years. A visit to Africa is thus, in other words, a visit to our planet’s past. There is one other significant strand to the story of mammalian evolution that sets Africa apart from other continents: it is the birthplace of our own species. We humans can trace our ancestry back through six million years of evolution in Africa and our history is inextricably linked with the history of this continent. This also means that the fauna and flora of Africa have evolved alongside us, having adapted to our presence. By contrast, other continents have had Homo sapiens rudely thrust into ecosystems that had, until then, evolved entirely without us. We arrived, fully armed and without notice, wreaking havoc on native species and introducing factors such as fire into systems that had not evolved to absorb them. Understanding African ecosystems provides us with far more than a mere appreciation of one continent’s biodiversity; it also offers us insights transferable to other continents, giving this subject a potential global importance. It is for this reason that I have written this book. I hope that you enjoy it!

3

CHAPTER

1

A Continent of Plenty

A

frica is home to an impressively diverse array of lifeforms. These, in turn, have generated some of the world’s most spectacular ecosystems. On a large scale, many need little introduction. Imagine herds of antelope and zebra migrating across Tanzania’s Serengeti grasslands, tailed by lions and other predators. Picture the wealth of bird life in the wetlands of Botswana’s Okavango Delta; the profusion of colourful fish on a coral reef off the coast of Mozambique; the uniquely adapted plants thriving on the rugged peaks of the Ethiopian highlands. On a smaller scale, peer into any patch of vegetation and you will find a multitude of insects and spiders. Lift a rock and you will probably discover centipedes, millipedes and perhaps a scorpion. Walk past a puddle at night and you may hear a cacophony of male frogs calling out to mates. Much of this diversity will be unfamiliar, however. Not just to you, but to experts too. Did you know, for example, that there are more than 100 species of shrew in the genus Crocidura, making this the most diverse mammalian genus in Africa? Were you aware that the continent is home to two species of elephant and four species of giraffe? Have you heard of the angwantibo? Or the three aquatic species of otter-shrew? Or the African ‘flying squirrels’, more correctly known as anomalures? These are just a few examples from an animal group usually considered well known: the mammals. As these examples suggest, Africa’s fauna is both diverse and relatively little known. But how diverse, exactly? And how does Africa’s diversity compare

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with that of other continents? These are the questions that this chapter aims to answer.

SPECIES RICHNESS IN AFRICA Let us ask a simple question: how many mammal species occur in Africa? Of course, we could ask the same question about birds, reptiles, spiders, grasses or any other group of organisms. Although such a question appears to be simple, in practice it is not so easily answered. In fact, it may surprise you to discover that we don’t actually know the answer. Perhaps rephrasing the question would help – and, at the same time, offer a little more insight into the issue. We could, instead, ask how many species of African mammal have been formally described by scientists. This is slightly easier to answer but still requires some discussion. What do we mean by ‘Africa’? How exactly do we define a ‘species’? It further requires an intimate knowledge of the scientific literature, as there is no central repository for storing scientific descriptions of new species. Let us start by defining what we mean by ‘Africa’. Essentially, this is an exercise in drawing boundaries. For the most part, the mainland African continent is easy enough to delineate. However, we need to bear in mind that unlike, say, Australia, Africa is linked to another continent, Eurasia, its connection to that continent preserved via a land bridge in Arabia. True, the Suez Canal, dug by human hands, now serves as a barrier for many organisms, but we need to remember that until it was completed in 1869, no such physical break existed between Africa and Arabia. In any case, this channel, which is 205 metres wide and 193 kilometres long, can hardly be considered a barrier to the movement of many organisms: birds and insects can fly across it with minimal effort; frogs, reptiles and small mammals may occasionally and inadvertently raft across it on floating vegetation. Nonetheless, the Suez Canal serves as a convenient boundary and, for present purposes, we will recognise it as the north-eastern limit of mainland Africa. In addition to mainland Africa, we also need to include a number of offshore islands closely associated with the continent: the Canary Islands, the islands in the Gulf of Guinea, Madagascar, the Comoros, the Seychelles archipelago and the Mascarene Islands are all traditionally viewed as part of Africa (figure 1.1). (See chapter 4 for more about island faunas.) 6

Tunisia Morocco Algeria Libya Western Sahara

Cape Verde

Mauritania

Senegal Gambia Guinea Bissau Guinea Sierra Leone Liberia

Egypt

Mali

Niger

Chad

Eritrea

Sudan Burkina Faso Benin Nigeria Togo Ivory Coast Ghana Cen African R Cameroon

Djibouti Somaliland South Sudan

Somalia

Eq Guinea Sao Tome

Ethiopia

Uganda

Gabon R Congo Rwanda Dr Congo Burundi

Kenya Seychelles

Tanzania

Comoros

Angola Zambia

Malawi Mozambique

Madagascar

Zimbabwe Namibia

Mauritius

Botswana Eswatini Lesotho

South Africa

0

Figure 1.1. Map of Africa and associated islands.

500

1000 km

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We now need to define what is meant by a scientifically described species. For a group of organisms to be recognised as a valid species, the taxon requires a formal description.1 At a minimum, this involves giving it a scientific name and a description of its features, such as its anatomy or behaviour, so that it can be differentiated from other closely related taxa. This topic is covered in chapter 2 and I will not dwell on it now, except to say that just because a formal taxonomic description exists does not mean that the taxon is valid. In some cases, it may already have been described in an earlier publication overlooked by the person defining the new taxon, meaning that the same species gets described twice. Not only has this happened numerous times in the past; it still happens regularly today. In such a situation, experts in the science of biological classification (taxonomists) give priority to the earlier name, with the later name(s) falling into synonymy, which is the process of subsuming different scientific names of the same taxon. An alternative scenario, also encountered frequently, occurs when the new description turns out to be incomplete or inconclusive and, on re-evaluation, the taxon cannot be distinguished from another closely related taxon. In such a case, the newly named taxon is once again subsumed into synonymy. An example of this process of taxonomic changes relates to vlei rats of the genus Otomys. Two species of vlei rats were described by Austin Roberts two years apart in 1929 (O. saundersiae) and 1931 (O. karoensis) from what are now the Western Cape and Eastern Cape provinces of South Africa, respectively. Then two decades later, in 1951, Roberts synonymised karoensis under Otomys saundersiae, which remained the prevailing wisdom until molecular techniques became available (see Taylor et al. 2005 for a history of these early name changes). Then in 2009, Peter Taylor and his colleagues showed that Otomys saundersiae was in fact nothing more than a colour variant of Otomys irroratus, while Otomys saundersiae karoensis was a separate species altogether (Taylor et al. 2009). Today, the name saundersiae does not describe a species of Otomys any more, while Otomys karoensis is regarded as a valid species and quite distinct from Otomys irroratus. With these terms defined, we are better placed to answer the question of how many described species of mammal have been recorded in Africa. For the sake of simplification, let us begin by considering one of the offshore islands: Madagascar. This is a discrete landmass with a clear oceanic boundary and, although large for an island, it is tiny by comparison with mainland Africa, 8

A Continent of Plenty

so we can more easily imagine a comprehensive coverage of the species of mammals that occur there. How many mammal species occur in Madagascar? Now we are faced with another problem, the fact that new species are constantly, and rather rapidly, being described. So, today’s answer is different from last year’s, which, in turn, is radically different from that of a decade ago. Let us look at this more closely. In a landmark 1995 paper, R.L. Peterson, J.L. Eger and L. Mitchell listed 27 species of bat from Madagascar (Peterson et al. 1995). This figure was revised upwards by 38 per cent to 43 species in 2011 by Steve Goodman (Goodman 2011). After more than two decades of intensive and focused taxonomic research on the region’s small mammals, Goodman described 20 new species of bat. The total figure for bat richness now rests at 46 species, but at least two potential additional species remain undescribed and so this figure will undoubtedly rise in the near future – perhaps even by the time this book is published.2 The island’s rodent and tenrec fauna demonstrate a similar increase in species richness. The bible for mammalogists is Mammal Species of the World: A Taxonomic and Geographic Reference, edited by Don Wilson and Diane Reeder. This landmark volume, first published in 1993, with the most recent two-volume edition published in 2005, lists 21 species of tenrec and 14 species of rodent for Madagascar (Wilson and Reeder 2005). Goodman, collaborating with Voahangy Soarimalala, increased the number of tenrec species to 32 and the number of rodent species to 27, almost doubling the latter (Soarimalala and Goodman 2011). Our conclusion from this little book-keeping exercise is that we still do not know the exact number of described mammal species occurring in Madagascar, but we do know that we have vastly under-estimated it in the past. With this in mind, we turn to mainland Africa. Fortunately, we have a recent and excellent six-volume publication dealing exclusively with African mammals: Mammals of Africa (MoA), edited by Jonathan Kingdon, David Happold, Thomas Butynski, Michael Hoffmann, Meredith Happold and Jan Kalina (Kingdon et al. 2013). Here, the total number of mammal species listed is a hefty and respectable 1 116, accounting for roughly one-fifth of all mammals on Earth. This encyclopaedic work was published in 2013, so we could be excused for thinking that the total figure cannot have changed much since then. But just two years later, in 2015, I was part of a team, together with Peter Taylor, Christiane Denys and Woody Cotterill, that published a book on the rodents of sub-Saharan Africa 9

AFRICAN ARK

Figure 1.2. The Southern African vlei rat (Otomys auratus). Photograph by Ara Monadjem.

(Monadjem, Taylor et al. 2015), in which we added dozens of new species. For example, 17 species of vlei rats, in the genus Otomys (figure 1.2), are recognised in MoA; we listed 31 species. MoA lists 5 species of Dasymys (marsh rats) and 15 species of Lophuromys (brush-furred rats) compared with 15 and 34 species, respectively, in our book. It is clear that the pattern of rising species richness I described in the microcosm of Madagascar plays out across the entire continent. As a result, we are nowhere near a definitive answer to the question of how many mammal species occur in Africa. Yet we may have a good enough picture to compare mammalian diversity in Africa with that in other regions globally.

AFRICA’S DIVERSITY IN A WORLDWIDE CONTEXT How does the number of mammal species in Africa compare with the numbers found on other continents? This, again, is difficult to answer. Africa is still

10

A Continent of Plenty

decades away from compiling a comprehensive list of its mammal species; most African regions have only been superficially surveyed, and some remote destinations have never even been visited by a mammologist (mammal expert). Even in well-surveyed countries such as South Africa, new species continue to be described (Taylor, Stoffberg et al. 2012). Broad-scale comparisons between Africa and continents such as North America, which have been the subject of detailed and comprehensive study for centuries, can thus be dangerously misleading. Furthermore, Africa suffers from a critical shortage of professionally trained and actively employed taxonomists. Taxonomists make a living by categorising and naming the living world. At the most basic level, they identify and name species, an activity that forms the very basis of biology: practically nothing useful can be studied in biology without reference to species and, by default, to their names. Yet there are very few working taxonomists on the continent. As a consequence, African animals, plants and other organisms are still predominantly being described by scientists based in Europe or North America. But to return to our original question: how does African mammal diversity measure up in a global setting? According to the latest published count, Africa boasts 1 116 species of non-marine mammals (Kingdon et al. 2013), increasing to 1 320 species if we include Madagascar. For simple comparison, here are the figures for some other continents: • • • • •

North America: 417 species South America: 1 264 species Europe: 219 species South and South East Asia: 1 281 species Australia, Papua New Guinea and New Zealand: 502 species (IUCN 2019).3

Connor Burgin and colleagues enumerated mammal species across the world in a slightly different way. They took sub-Saharan Africa and associated islands as the ‘Afrotropical’ realm, which they compared with the other so-called zoogeographical regions of the world: the Neotropics (essentially South and Central America, and the Caribbean); the Palearctic (Eurasia, Japan and north Africa); the Nearctic (North America), Indomalaya (South and South East Asia); and Oceania (Australia, New Zealand, Melanesia, Micronesia and Polynesia). In terms of this arrangement, species richness rose to 1 572 for the Afrotropics, and compared with other regions as follows:

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• • • • • •

Neotropics: 1 617 species Afrotropics: 1 572 species Palearctic: 1 162 species Indomalaya: 954 species Nearctic: 697 species Oceania: 527 species (Burgin et al. 2018).

By this measure, Africa remains a diverse continent – though it is not the most diverse one. Another way to measure mammalian diversity is to count the number of higher taxa. Species offers one level of taxonomic categorisation, but we can also count at a higher taxonomic level within the class Mammalia, for example at the level of genus (plural = genera), family or order (see Table 2.1 in chapter 2). Such an approach allows us to view diversity from a different angle. It is true that species are the only ‘real’ taxonomic entities, in the sense that plants and animals differentiate between their own species and others – for example, by mating only with their own species. By contrast, a genus is entirely a human construct, allowing us to order and arrange biological diversity in a hierarchical fashion – the so-called Linnaean hierarchy – for ease of information retrieval (see chapter 2). However, plants and animals have no notion of these higher taxonomic groupings. A lion, for example, will not treat a leopard or tiger (all members of the genus Panthera) differently from, say, a cheetah (genus Acinonyx) based on generic status – though it may, of course, treat them differently on, for example, ecological grounds. By counting genera, families or orders, we are able to compare diversity at a deeper level. Take a rapidly evolving genus that produces multiple, similar-looking species: since the genus is evolving rapidly, we can assume that the different species will be similar because they will not have had the time to accumulate more noticeable differences. Now imagine a landscape with five such speciose (that is, species-rich) genera. At the species level, diversity in this landscape will be high, because each genus contains numerous species. However, at the genus level, diversity is low because there are just a handful of genera. At the level of family and order, diversity may be even lower. For instance, all five genera in this imaginary example might belong to just two families, both of which belong to just one order.4 Now take another landscape with a similar number of species but categorised into a greater number of genera (each genus thus having fewer

12

A Continent of Plenty

species than in the previous landscape), in more families and in several orders. How should we compare these two landscapes? Each has the same number of species, but clearly there is ‘deeper’ diversity in the second landscape that has more genera, families and orders. One way of visualising this difference is by viewing each of the two landscapes as a tree with the terminal twigs representing species, the smaller branches representing genera, the larger branches depicting families, and the main boughs portraying orders. The two trees would have the same number of twigs, but the first landscape would have fewer branches and a single bough, whereas the second landscape would have more branches and perhaps two or more boughs. This greater diversity will be evident and measurable in the greater structural and/or anatomical diversity of the mammalian community in the second landscape. This is simply because different species in the same genus will possess more-or-less the same morphological features (think of the black wildebeest [Connochaetes gnou] and blue wildebeest [C. taurinus]), whereas genera in the same family can be strikingly different (compare wildebeest with the reedbuck genus Redunca). Families and orders differ even more. So, let us repeat those comparisons between continents, using the same sources as before, but this time at higher taxonomic levels. There are 333 genera in 66 families and 14 orders of mammals in Africa. (If we include Madagascar, the first two figures increase greatly, but the number of orders remains the same.) The comparable numbers on the other continents are outlined in Table 1.1. What does this tell us about diversity in Africa? At a species level it is relatively high, Table 1.1. Numbers of mammalian species, genera, families, and orders (including marine mammals) found in each of the six zoogeographic regions of the world. Zoogeographic region

Species

Genera

Families

Orders

Afrotropics

1 572

333

66

14

Neotropics

1 617

377

54

14

Palearctic

1 162

281

53

10

954

248

51

13

Indomalaya Nearctic

697

185

36

11

Oceania

527

209

38

11

Sources: The number of species per region was taken from Burgin et al. (2018). The remaining values were extracted from the Mammal Diversity Database (Upham 2020).

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but not significantly different from species levels in South America and South and South East Asia. At higher taxonomic levels, however, we see that Africa stands out as having more families of mammal than any other continent. Our conclusion from this rough tabulation is that Africa has a rich and deeply varied mammalian fauna.

FUNCTIONAL DIVERSITY We may well marvel at how diverse African ecosystems are. However, diversity is more than just a list of species, families or orders. There is another level at which we can view diversity, which entails examining the ecological roles that African mammals perform and seeing how varied these roles are. Consider, for example, the humble aardvark (Orycteropus afer). This sole descendant of an ancient African lineage, the Afrotheria (see chapter 3), lives exclusively on a diet of ants and termites, which it digs up from their nests and mounds. Try digging into a termite mound and you will soon discover that these structures are as hard as nails, resisting even picks and shovels. An aardvark, however, is a veritable digging machine, using its massive claws and strengthened forelimbs to break through to the inside of the mound. This adaptation enables the aardvark both to feed and to make a burrow for itself. However, the beneficiaries of the aardvark’s digging skills include many other completely unrelated organisms. A recent study at three South African sites (Whittington-Jones et al. 2011) counted a total of 21 mammal species utilising aardvark burrows as shelters, including many species of rodent, several carnivores, the scrub hare (Lepus saxatilis) and the African warthog (Phacochoerus africanus), not to mention two birds (a swallow and a chat), three reptiles (all lizards) and an amphibian (a toad). This count was done in just one region of South Africa and does not include insects and other invertebrates, so imagine the hundreds of species that must rely on aardvarks across the rest of the continent. Aardvarks are thus restructuring the environment in such a way that a whole suite of other organisms benefits from their activity. In short, they are ecosystem engineers: through their diggings they provide valuable ecosystem services without which many other species would either decline in number or disappear entirely. Organisms such as the aardvark are known as ‘keystone species’, by analogy with the central stone in a traditional arched bridge: take this stone away and the 14

A Continent of Plenty

rest of the building blocks crumble and collapse. Africa is home to numerous such species, all of which provide critically important ecosystem services. The best-known is the greatest engineer of them all, the African savanna elephant (Loxodonta africana). Savanna elephants, unlike forest elephants (Loxodonta cyclotis), typically inhabit open habitats where grasses and trees compete for dominance. But viewing the relationship between the elephant and its habitat in this way, with the elephant as a beneficiary of a pre-existing habitat, misses an important point. It assumes that environmental factors such as rainfall or soil type determine the structure of a habitat. In fact, biotic (that is, biological) factors, such as the actions of herbivorous mammals, are equally important. Elephants create their own habitats. By pushing over trees and uprooting shrubs, they can alter the structure of a woodland and turn it into a grassland (figure 1.3). Perhaps the best-known example of this is Tsavo National Park in Kenya. Wooded in the 1940s, this habitat began opening up in the 1960s with elephant numbers on the rise, and by the early 1970s it had been converted to a grassland. A similar story can be told for the Maasai Mara National Reserve, also in Kenya: now a famous grassland, it was largely wooded terrain a few decades ago.

Figure 1.3. Trees pushed over by elephants in the Maasai Mara National Reserve, Kenya. Photograph by Ara Monadjem.

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The ecological role of elephants has generated a lot of debate, much of it fiercely partisan. Some researchers highlight the destruction of vegetation caused by elephants, arguing that this is detrimental to both the flora and the animals that rely on this vegetation for cover. Others convincingly claim that elephants are a natural component of savanna ecosystems and that the destruction we see is nothing more than our anthropocentric interpretation of the extreme state in a natural long-term cycle. Elephants are not destroying habitat, argue the proponents of this claim: instead they are shifting it spatially over long periods of time, creating heterogeneity and thus ultimately allowing a greater number of species to coexist than in a non-fluctuating system without elephants. This has caused a real, and slightly alarming, divide in some conservation quarters, with one set of voices calling for elephant control measures in areas where numbers are high, while an opposing set of voices demands that elephants be left untouched. The controversy over elephant ecology has been eloquently reviewed by Bob McCleery, wildlife ecologist extraordinaire from the University of Florida in the United States (see chapter 6). McCleery has dubbed this the ‘elephant paradox’, and it can be understood as follows. Savanna elephant populations are in decline, and the species will not survive into the future without our protection. In addition, elephants play a critical role in savanna ecosystems by, for example, controlling woody plant encroachment (which has been ranked as one of the most pernicious threats to savanna systems globally). However, where elephant numbers have risen through protection, they denude the savanna, leading to measured losses in biodiversity. Thus, where elephants have been extirpated, the habitat is in trouble; where elephants have been successfully protected, the habitat is in trouble. We will revisit the elephant paradox in chapter 6. Next, I would like to examine one group of mammals that provide valuable – and largely overlooked – ecosystem services: bats. Bats are intriguing for a whole set of reasons, including their ability to fly (birds and the extinct reptilian pterosaurs are the only two other vertebrate groups to have evolved flight) and their ability to perceive their environment through echolocation (‘seeing’ with their ears). However, here I would like to emphasise how bats, by consuming tons of insect pests, are an essential component of any crop-farming operation. To say that bats are ‘farmers’ friends’ is to dramatically understate their importance: friends provide a shoulder for you to cry on; bats save farmers US$3 billion in pesticide costs annually in the United States alone (Boyles et al. 2011). 16

A Continent of Plenty

And they also provide two other vital ecosystem services: plant pollination and the dispersal of fruits. Most of the seminal work on bats and ecosystem services has been conducted in the United States, with other important studies being done in Europe and South America. Very little such research has taken place in Africa. The first studies of bats and ecosystem services in Africa, in which I was fortunate enough to play a part, were conducted in Eswatini, led by two Danish master of science (MSc) students, Kristine Bohmann and Christina Noer (figure 1.4). Together, we investigated the movement ecology and diet of two species of open-air foragers: the Angolan free-tailed bat (Mops condylurus) and the little free-tailed bat (Chaerephon pumilus). Noer fitted 20 individual bats with tiny transmitters that emit radio-wave signals, and released the animals unharmed back into the environment at the point of capture. These signals can be picked up by an antenna attached to a receiver. The team followed each animal over

Figure 1.4. Kristine Bohmann (left) and Christina Noer (right) testing the telemetry equipment used to track molossid bats in the Simunye region of Eswatini. Photograph by Ara Monadjem.

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multiple nights as it left its roost, in the roof of a house, and made its way to its foraging area. By recording the compass direction and strength of the signal, Noer was able to determine the location of each bat to an accuracy of 50 metres. Bohmann, meanwhile, was quantifying the diet of these bats. Traditionally, diet studies on small mammals have either examined stomach contents or picked through faeces in search of identifiable insect body parts, such as legs or wings. Neither approach yields very precise data. Furthermore, the stomach contents approach requires ‘sacrificing’ the animal. Instead, Bohmann applied cuttingedge molecular biotechnology – ‘next generation sequencing’, as it is known – to address her question. Essentially, she collected fresh faeces from bats as they returned to their roost after an evening’s foraging, and then sifted through the DNA in the faeces to see what had been eaten. This is not as easy as these few sentences make it sound, and Bohmann needed the help of Tom Gilbert, a leading molecular ecologist specialising in ‘ancient DNA’ (such as DNA extracted from bones of extinct animals). This work was conducted in Gilbert’s laboratory and under his supervision, at the University of Copenhagen in Denmark. The results of these two parallel studies were astounding. Noer showed that the bats preferred to feed over sugarcane fields, shunning altogether the natural savanna that was available in abundance. Further, these two tiny bat species (little free-tailed bats weigh around 12 grams and Angolan free-tailed bats around 24 grams) flew up to 10 kilometres each night from roost to foraging site, and then back again (Noer et al. 2012). Another interesting finding was that the bats finished feeding and returned to the roost within a two-hour period, suggesting that they are highly efficient predators. The preference of these free-tailed bats for foraging over sugarcane habitat was independently established by an MSc student of mine, Fezile Mtsetfwa. Mtsetfwa took a different approach to quantifying habitat preferences of bats in this region by placing bat detectors across the landscape. In this way, she was able to show that free-tailed bats prefer to forage over sugarcane by severalfold more than over native savanna (Mtsetfwa et al. 2018). Bohmann’s study was equally insightful. She showed that both species preferred moths, flies and bugs as food, and their diet included several sugarcane pests such as moths of the genera Eldana and Mythimna (Bohmann et al. 2011). Our conclusion was that bats should most certainly be investigated as agents of pest suppression in a southern African agricultural setting. However, as is so often the case, I was unable to find funding to continue with this preliminary work and had to put my ideas on the backburner for more than half a decade. Luckily for us, the 18

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story was taken up by Peter Taylor who was working in the Vhembe Biosphere Reserve in Limpopo Province in northern South Africa. He secured funding to experimentally test the impact of bats and birds on pest insect populations in macadamia nut orchards, and the damage these insects cause. This work has only recently been completed, providing evidence that bats do indeed have a significant effect. I will discuss Taylor’s work in chapter 9, when we look more deeply into the role of small mammals in agricultural settings. Scavenging animals suffer from an undeserved bad reputation. We are repulsed by the apparent gusto with which a hyena or vulture attacks a bloated, stinking carcass. But what would happen if these scavengers did not feast on the deceased? A dead herbivore, such as a wildebeest or a cow, provides nourishment for hundreds of thousands, if not millions, of maggots. These will pupate into adult flies, causing great misery for humans, unless the carcass is disposed of quickly enough by hyenas, jackals and vultures. Rather than malign these scavengers, we should treat them with respect and awe and award them the top environmental prize for free clean-up services! Among the scavenging tribe, the greatest heroes are vultures. Although hyenas are generally regarded as scavengers by most laypersons and are well adapted to feed on any carcasses that they find, they actually hunt a large proportion of their own food – particularly in open habitats such as the Serengeti ecosystem. Similarly, jackals may enjoy the occasional carcass, but they also hunt small mammals such as rodents, and supplement their diet with insects and fruits – the amount of energy they derive from scavenging varying markedly from one individual to another. Vultures, by contrast, are obligate scavengers. Indeed, they are the only vertebrates to derive their entire energy budget from scavenging carcasses, mostly those of dead mammalian herbivores. In a book about mammals, it might be considered remiss of me to devote several paragraphs to birds. However, vultures are one of my favourite study animals, and doing so enables me to make an important point below about ecological connections and the impact that these may have on humans, so I hope that you will indulge this slight digression. And, as you will see shortly, our digression on vultures eventually leads back to mammals! Vultures do not form a single taxonomic unit. The term ‘vulture’ is, rather, an ecological one, bringing together several groups of bird that share a scavenging lifestyle and associated morphological features. For example, the Old World (Africa, Europe and Asia) and New World (the Americas) vultures are not closely related to each other: an Old World vulture such as the African 19

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white-backed vulture (Gyps africanus) is more closely related to the eagles than it is to, say, the turkey vulture (Cathartes aura) of the Americas. Even within the ten species of African vulture, some relationships are relatively distant: the genera Gyps, Torgos, Aegypius, Necrosyrtes and Trigonoceps form a neat clade (a group of organisms sharing a recent common ancestor), whereas the genera Gypaetus, Neophron and Gypohierax form a separate unrelated clade allied to the non-scavenging African harrier-hawk (Polyboroides typus).5 The biology of African vultures is beautifully presented in The Vultures of Africa by Peter Mundy, Duncan Butchart, John Ledger and Steven Piper (Mundy et al. 1992). Much of what we know about vultures is encapsulated in this book. In the three decades since its publication, however, we have come a long way in studying these wonderful creatures, with new technology and analyses helping to generate a flood of new information and insights – particularly through the fitting of transmitters that allow automated tracking of the birds via satellites or the cellular telephone network. We now know, for example, that Gyps vultures (which comprise all the species with long, sinuous necks, viewed by most people as ‘typical’ vultures) travel enormous distances

Figure 1.5. An African white-backed vulture (Gyps africanus) in flight in the Maasai Mara National Reserve, Kenya. Photograph by Ara Monadjem.

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in search of carrion (figure 1.5). In one study conducted in Namibia in which I participated, together with one of my former PhD students, Andy Bamford, and several other co-authors, we showed that five Cape vulture (Gyps coprotheres) adults had a mean home range of 21 320 square kilometres (Bamford et al. 2007), an area larger than the largest protected area in that country and larger than the whole area of my home country, Eswatini. Subadult birds, not being attached to a nest site, roamed much larger areas of around 500 000 square kilometres (equivalent to a medium-sized African country such as Kenya), an order of magnitude larger than the area covered by adults. With another former PhD student, Adam Kane, we showed that adult Cape vultures roam across 100 000 square kilometres of South African grasslands, with immature vultures covering three times as much ground (Kane et al. 2016). These huge distances that vultures travel make sense when one considers that their food consists predominantly of the carcasses of large herbivores, both wild and domestic. A single carcass can feed many birds, but the birds have to cover an extensive area to find one. This, of course, has serious conservation implications: how do you conserve an animal that effortlessly crosses boundaries from the relative safety of parks and reserves to areas beyond, where it may be shot or poisoned, or collide with powerlines (Ogada, Keesing and Virani 2012; Ogada, Shaw et al. 2016)? Furthermore, these animals move across international boundaries, often rendering national policies for their protection ineffective. Vultures, more than any other animal, call into question the sometimes hard-nosed ‘conservation by protected area’ approach rampant in much of Africa. Obviously, national parks and other protected areas are fundamental tools for conservation, but they cannot in themselves stem the tide of extinctions that is eroding our global biodiversity. We need to look beyond the national parks paradigm. I address this issue further in chapter 10. I have one further point to make about vultures, and that concerns their role in reducing contact between mammalian carnivores. They do this by consuming carcasses quickly, before jackals and hyenas can get to them. Thanks to their wings, vultures can scour far greater areas than mammalian scavengers can on foot, and therefore generally find carcasses earlier. Once found, a single adult impala carcass can be picked clean by a phalanx of vultures in just eight minutes. That does not leave much time (or food) for a hyena or jackal. As a result, where carcasses are available to vultures, fewer jackals, hyenas and feral 21

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dogs visit the carcass. So why is this of importance to us? The reason lies in the transmission of diseases, such as rabies, a virus that is deadly to humans. The dog family (Canidae) is a reservoir for this virus, and increased contact between canids increases the chances of transmission of rabies between the reservoir populations. This, in turn, increases the chances of rabies being transmitted to humans. The details of this transmission process were confirmed by Darcy Ogada working in Kenya (Ogada, Torchin et al. 2012). Exactly such a scenario has played out in India in the wake of the Asian vulture crisis of the 1990s and 2000s, in which around 99 per cent of the region’s vultures were killed by veterinary medication used for cattle, the non-steroidal, anti-inflammatory drug diclofenac. This happened quickly, in less than ten years, and by the late 1990s literally millions of vultures had disappeared. Prior to their demise, vultures had been responsible for disposing of cow carcasses in India; with their disappearance, feral dogs rapidly increased in number as they benefitted from the greater supply of carcasses, resulting in an increased incidence of rabies cases in humans.

AFRICAN ECOSYSTEMS The archetypal African landscape of popular culture is a vast grassy plain dotted with characteristic acacia trees. Savannas, as such landscapes are called, cover around 60 per cent of the continent and represent a dynamic interaction between several driving forces, including rainfall, underlying soils, herbivory (particularly by megafauna) and another consumer of plant biomass, fire. As such, savannas are not ‘climax’ associations; climax vegetation refers to plant communities which, if the drivers are allowed to run to their natural conclusion, result in stable habitats, such as certain types of forests. If you cut down a tropical rainforest, for example, then sit back and watch, you will see (if you live long enough) the forest regenerate over time, passing through several ‘successional’ stages, from a scruffy tangle of thickets to a secondary forest dominated by pioneer species, and finally returning to primary (or climax) forest after several decades or even centuries. This is a relatively predictable process, as long as the plants are allowed to regenerate. Of course, the primary forest will not regenerate if people continue to log trees as they mature or set fire to the thickets annually. 22

Ecosystems Aquatic Desert Dry forest Fynbos Karoo Mediterranean Montane Rainforest Savanna

0

750

1500 km

Figure 1.6. Map showing major African ecosystems based on the Terrestrial Ecoregions of the World (Olson et al. 2001).

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Savannas Savannas do not represent a ‘primary’ or ‘climax’ stage. They are not the end products in a successional sequence of plant communities, but are dynamic and continuously changing, opening up into grasslands or closing in to become woodlands. For this reason, it does not make sense to talk about the ‘natural’ condition of a savanna. There is no such thing as a ‘pristine’ savanna, at least not in the same sense that we can talk about ‘pristine’ rainforest (although even there, we would be well advised to avoid the word: in a constantly evolving world, does ‘pristine’ ever convey anything of scientific value?). We can talk about the utility of a savanna, however. For example, a cattle rancher might consider a savanna degraded because of reductions in its potential forage production. But we need to be very careful before we make absolute statements about its ecological integrity. Such statements necessarily follow value judgements made collectively by society. If our society expressly wishes to conserve elephants, then we will judge a savanna by different standards from those societies where the primary goal is to conserve the maximum number of species, maintain the greatest number of ecological processes, or harbour a selection of iconic habitats. We can only judge the value of a savanna through the lens of each of these different goals. This is the main cause of the often heated disagreements between ecologists over the status of African savannas, and explains the perennial debate surrounding the impact of elephants. Given the protracted nature of this dispute, the general public could well be excused for thinking that ecologists don’t really understand savannas. This is not, in fact, correct. Although we have much to learn about the dynamics of African savannas, we are not as ignorant as we might appear. Much, if not all, of the disagreement would dissipate if we recognised the simple fact that savannas are dynamic ecosystems that have evolved to deal with such constantly changing conditions. Forests and deserts Africa has two other extensive ecosystems: forests and deserts. The Congo Basin lies in the heart of Africa and influences the climate across most of the region. Stretching from the Albertine Rift (the western branch of Africa’s Great Rift Valley) in the east to the western seaboard, and straddling the Congo River, this is the second-largest tract of lowland rainforest in the world after the Amazon. Rainforests extend deep into West Africa too, with the Upper Guinea rainforest having once covered much of the region from Ghana to Sierra Leone, although 24

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it is today greatly fragmented and modified. The Lower Guinea rainforest, by comparison, is still relatively intact across Cameroon and Gabon. Small isolated tracts of rainforest also occur in east Africa, such as the Kakamega Forest in Kenya, but this region is predominantly savanna because of the mountains of the Albertine Rift, to the west, which prevent moisture-laden rain clouds from the Congo Basin from penetrating here. Lowland rainforests are the planet’s greatest biodiversity hotspots and Africa’s rainforests are no exception. The diversity of animals and plants they harbour far outweighs that of any other ecosystem, with interesting exceptions, of course: terrestrial tortoises reach their peak richness in arid regions of southern Africa, and the fynbos floral kingdom in South Africa’s Cape region has more species of plants per unit area than anywhere else in Africa. However, Africa’s rainforests drip with bird and mammal diversity. Mount Nimba, straddling Liberia, Guinea and Ivory Coast, covers just 674 square kilometres (one-third the size of South Africa’s Kruger National Park) and is poorly studied, yet it harbours at least 59 species of bat, most of which are forestdependent (Monadjem et al. 2016). Another relatively poorly documented area is Comoé National Park in Ivory Coast, which covers 11 500 square kilometres and has 57 species of bat (Fahr and Kalko 2011). Compare this with the 73 bat species known from the enormous country of Mozambique, or the 63 species known from the even larger and better studied South Africa, and we get some idea of the richness of lowland rainforests. Mozambique and South Africa, of course, extend across a huge environmental gradient, so have a much greater diversity of habitats than the two west African rainforest sites. A more meaningful comparison might thus be between Mount Nimba and Comoé and a similar-sized area of savanna. Gorongosa National Park in Mozambique provides just such a comparison, and has been surveyed at least as well as the two rainforest sites. Just 38 bat species from here are known.6 Comparing equatorial rainforests with the more temperate forests further south is also instructive. A PhD study by Monika Moir (Moir et al. 2020) recorded just 25 species of bat from 17 forests across the Eastern Cape and KwaZulu-Natal provinces of South Africa. Regardless of which small mammal group we investigate, we reach the same conclusion: tropical rainforests produce greater diversity than savannas. A ­typical rainforest site will be home to between 10 and 20 species of shrew, for example, whereas a similar site in savanna will usually support fewer than 5 species. 25

(a)

(b) Figure 1.7. Ecosystems discussed in this book. (a) Savanna (Serengeti National Park, Tanzania), (b) forest (Bwindi Impenetrable Forest, Uganda), (c) desert (Namib Desert, Namibia) and (d) mountains (Malolotja Nature Reserve, Eswatini). Photographs by Mike Unwin.

(c)

(d)

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There are three species of pangolin in some African rainforest sites; savannas have just one. Rodents, too, are more diverse in rainforests than in savannas. A few groups of larger mammals do provide exceptions to this rule: zebras, rhinoceroses and other larger ungulates (in particular the bovids), together with the large predators that feed on them (cats, dogs, hyenas), exhibit greater richness in Africa’s savannas than in its forests. Yet even here, there are some reversals – such as with duikers, which show greater species diversity in rainforests. And some groups, such as buffalos, elephants and pigs, appear equally distributed between both ecosystems. The world’s largest desert system occurs in Africa: the Sahara. Two other deserts cover extensive areas of south-western Africa (the Namib, mostly in Namibia but extending marginally into Angola in the north and South Africa in the south) and the Horn of Africa (covering much of Somaliland, Somalia and Ethiopia, and extending marginally into northern Kenya). Deserts may appear to be harsh, forbidding places, but they host a fascinating array of arid-adapted species. And despite their vastness, many of these species are on the cusp of extinction. The addax (Addax nasomaculatus) is a large antelope, the size of a small oryx, with a whitish coat and long spiral horns. This majestic creature once roamed right across the Sahara, from the Atlantic coast in Mauritania to the Nile River in Egypt, and in numbers unimaginable today. As late as 1960, by counting tracks, more than 5 000 individuals were recorded in just one day (Kingdon and Hoffman 2013). However, the addax has been obliterated across its former range by uncontrolled and merciless hunting, made possible by modern rifles. Today, fewer than 300 individuals remain in two populations in remote and unprotected parts of Chad and Niger (and possibly a third in Mauritania), with reintroductions to reserves in Tunisia and Morocco. This would make the addax a strong contender for the most threatened large mammal in Africa, were it not for the long list of other such species; for example, the scimitar-horned oryx (Oryx dammah), a close relative of the addax in the subfamily Hippotraginae. This magnificent antelope once occurred in the semi-arid fringes of the Sahara right across the continent, again from the Atlantic to the Nile. It has since suffered such catastrophic population reductions that it has now effectively disappeared from its natural habitat. How many people today have ever heard of the scimitarhorned oryx? This species has not been recorded in the wild in almost three decades and is classified as ‘Extinct in the Wild’ by the International Union for 28

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Conservation of Nature (IUCN) (2019). Like the addax, the scimitar-horned oryx was once abundant, living in herds hundreds strong, but was driven towards extinction by the ignorance and greed of humanity. Unyielding hunting pressure saw populations in most range states go extinct in the 1950s and 1960s. Some 3 500 individuals survived in a protected area in Chad through the 1970s (Kingdon and Hoffman 2013), but by 1988 this population had dwindled to a few dozen animals at most, and two years later it was extinct. Fortunately, a captive breeding programme was under way before the demise of this species in the wild, and these stocks have since formed the nucleus of reintroduction efforts in Tunisia, Morocco and Senegal. Three other ecosystems deserve our attention here for their biological diversity and endemism, even though the absolute numbers they harbour may not be as spectacular as those of forests or savannas (either in terms of species richness or extent of coverage): upland habitats created by mountains; freshwater aquatic habitats; and the fynbos at the southern tip of the continent. I will deal with them in this order. Upland habitats Mountains and upland regions are not uniformly distributed across the continent. For example, west Africa, from Nigeria to Senegal, has only a few low mountains (not extending much beyond 2 000 metres above sea level) restricted to a handful of countries. This vast region, therefore, is practically flat, and those mountains that do exist are not particularly lofty. The situation is reversed in east Africa. Here, mountains and mountain ranges predominate, and stretches of flat lowlands are difficult to find, except close to the coast. What is more, these mountains reach great heights. The isolated peaks of Mount Kilimanjaro and Mount Kenya tower 5 895 metres and 5 199 metres respectively above sea level, while the mountains on either side of the eastern rift valley in Ethiopia regularly level out at an elevation above 4 000 metres, forming the largest continuous block of highlands anywhere in Africa. In the Albertine Rift – a geological fault line that extends from the boundary between the Democratic Republic of the Congo (DRC) and Uganda in the north, southwards through Rwanda and Burundi to the western extreme of Tanzania – the Ruwenzori Mountains rise to more than 5 000 metres above sea level. From here, mountain chains extend all the way south through Tanzania, 29

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Malawi, Zambia, Mozambique and Zimbabwe to South Africa, forming part of the extensive Afromontane ecosystem. Other important upland areas include the Cameroon Volcanic Line, a chain of mountains straddling the boundary between Cameroon and Nigeria; the highlands associated with the escarpment of western Angola; and various mountains deep in the Sahara, notably Hoggar, Tibesti and Aïr mountains. Mountain ranges, for reasons that we shall see in chapter 5, act as ‘species pumps’, with resulting high levels of endemism. An endemic species is one that has a distribution restricted to a defined geographical area, such as a mountain, a country, or a continent. For example, the Afromontane region of South Africa (and its tiny neighbouring states of Lesotho and Eswatini), harbours at least 14 species of bird found nowhere else in the world. Similarly, the highlands of Ethiopia host more than a dozen endemic bird species. By contrast, Zambia, a country of comparable size to Ethiopia but covered in savanna, supports just two endemics, the black-cheeked lovebird (Agapornis nigrigenis) and Chaplin’s barbet (Lybius chaplini), even though overall bird diversity is higher here than in the Ethiopian mountains. Among mammals, too, one finds astonishing endemism in the African highlands – all the more surprising, given how we are generally steered towards savannas and forests to view African mammals. Indeed, many groups of mammal have radiated widely within these upland habitats, extending at greatly reduced levels of diversity into the surrounding savannas and forests. Take the rodent genus Otomys (vlei rats), typically associated with rank grasslands at the edge of swamps or bogs: six species occur in the highlands of Ethiopia and another three species in the Albertine Rift, whereas just one species, the Angoni vlei rat (Otomys angoniensis), is widespread in savannas. However, Africa’s upland areas are not only rich biologically, they are also home to much of the continent’s human population. The soils tend to be fertile, the mountains trap moist air – which falls as rain – and the higher elevations harbour fewer of the diseases, such as malaria, that are so prevalent in the surrounding lowlands. It is thus here that the high pressure on natural resources and the high levels of endemism converge, resulting in a conservation nightmare (or opportunity, depending on how you view the world). Finding viable long-term solutions to conservation problems will not be easy, but any conservation plans will necessarily have to address, or at the very least include, the issue of how to improve the livelihoods of local communities. We will examine this topic in greater detail in chapter 10. 30

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Freshwater aquatic habitats Freshwater aquatic habitats include rivers, lakes, marshes and swamps, as well as dams and other artificial impoundments. Estuaries provide ecological links to marine systems and harbour many interesting plants, fishes and insects. Compared with savannas, forests and upland areas, these ecosystems cover a tiny proportion of the African continent, yet they are critical to the continued welfare of humanity. Most of the water we drink or use for domestic and industrial purposes comes from them, as does the water that we use to irrigate our crops or supply to our livestock. The fish they support are the main source of protein for millions of people on the African continent. Rivers and lakes have also fostered economic activity by making navigation possible between otherwise remote and disconnected localities. In a similar way, aquatic ecosystems link the various terrestrial systems through rivers, providing life-nourishing water and nutrients carried in silt or sediment. Quite apart from their value as ecological corridors, rivers and lakes are also important centres of biodiversity in their own right. Lake Malawi, for example, has more than 1 000 species of fish (90 per cent of them in the family Cichlidae), making it the most diverse wetland in Africa from an ichthyological perspective. Waterbirds such as cormorants, herons, ducks and storks play an important role in moving nutrients between aquatic and terrestrial ecosystems by feeding on fish and other aquatic lifeforms and then defecating on land, since most of these species roost and nest in trees. Africa’s rivers and lakes are also home to several interesting mammals. The best known is probably the hippopotamus – or, more correctly, the two species of hippopotamus, as the common hippopotamus (Hippopotamus amphibius) also has a smaller, rarer cousin, the pygmy hippopotamus (Choeropsis liberiensis), which is restricted to west Africa’s Upper Guinea rainforest. The former is widespread across the continent throughout the moist savanna zone, despite hunting having heavily depleted populations in many areas, and remains instrumental in many aquatic systems by creating channels (simply by regularly walking the same routes) and, like waterbirds, transferring nutrients – in this case mostly from terrestrial to aquatic ecosystems (see chapter 6). Hippopotamuses are vegetarians, feeding on grasses, which they harvest with their wide mouths in a similar manner to a lawnmower. This they do at night, probably to escape the heat of the African sun. They spend the daylight hours in water, or basking in the sun on sandbanks close to rivers, and, in the process,

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empty the nutrients harvested from a terrestrial ecosystem into an aquatic one. This influx of nutrients maintains ecosystem productivity, and the channels that hippos create keep the system dynamic; both processes are essential to the health of many African wetlands. Thus, the common hippopotamus is another ecosystem engineer par excellence, and plays a role in maintaining fish stocks that feed so many people in these regions. These ecosystem services should not be forgotten when we read scare stories describing the hippopotamus as ‘the most dangerous animal’ (killing the greatest number of humans) in Africa.7 The trick is to learn how to live with these huge herbivores so that we reduce their negative impacts, while at the same time maximising the benefits that they offer us. Hippopotamuses are not Africa’s only aquatic mammals. Others include the West African manatee (Trichechus senegalensis) of west and central Africa; several species of otter; two genera of otter-shrew (Potamogale and Micropotamogale), which have affinities with the tenrecs of Madagascar; several species of aquatic rat, of the genus Colomys, that inhabit tropical rainforests; the sitatunga (Tragelaphus spekii), a semi-aquatic antelope that occurs widely in wetland habitats throughout the tropical forests and savannas of central Africa; an aquatic genet (Genetta piscivore) restricted to the western portion of the Congo Basin; and the marsh mongoose (Atilax paludinosus). Many other mammal species are associated with riverine thickets or rank vegetation at the edges of wetlands. Fynbos Fynbos is, in some ways, the most intriguing of all African ecosystems. Covering no more than 46 000 square kilometres (an area the size of the Selous Game Reserve, Tanzania) and restricted to the extreme south-western tip of South Africa, this ecosystem supports 9 000 species of vascular plant, which represents some 20 per cent of all plant species recorded from Africa. How can this be? What is so special about this tiny area that it harbours such mind-boggling diversity? These riches are not simply botanical in nature. The fynbos also boasts an incredible diversity of insect forms, including high endemism. Moss frogs of the genus Arthroleptella have diversified extensively in the Cape Fold Mountains in the very heart of the fynbos and are in fact restricted to this region. Here is another example of undetected diversity: when Neville Passmore and Vincent Carruthers published their 1979 book South African Frogs, they recognised just three species in this genus. Three decades later, as a result of new research 32

(a)

(b)

(c) Figure 1.8. Ecosystems discussed in this book. (a) Aquatic (Zambezi River, Zimbabwe), (b) marine (humpback whale Megaptera novaeangliae, a regular sight off Africa’s Indian Ocean coast), and (c) fynbos (Blue Hill Nature Reserve, South Africa) (c). Photographs by Mike Unwin (aquatic, marine) and Ara Monadjem (fynbos).

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conducted by Andrew Turner, with whom I had the privilege of attending zoology classes at the University of the Witwatersrand in the late 1980s, and his colleague Alan Channing, the doyen of amphibian systematics in southern Africa, the number of species had increased to seven (Turner and Channing 2008) – and this in a region where many famous herpetologists have dedicated lifetimes to studying reptiles and amphibians. We can only imagine what awaits discovery in parts of Africa that have never seen a resident herpetologist. Mammalian diversity in the fynbos is rather modest compared with that present in other ecosystems; however, it is no less interesting. For example, Verreaux’s meadow mouse (Myomyscus verreauxii) is a 50-gram rodent endemic to the fynbos. This mouse is widespread and abundant within its distributional range – and this is basically all that was known about the species until it caught the attention of Jeremy Midgley. I once presented Midgley with a plump legless lizard of the genus Acontias (resembling a fattened Frankfurter sausage), his first question was not ‘what species is that?’ (which would have been my own primary concern) or ‘how did you catch it?’ Instead, he asked me whether it was poisonous. Not whether it was venomous, in the sense of a cobra that injects venom through its fangs (no African lizard has venom strong enough to harm humans), but whether it had poison in its skin. The question baffled me, so I asked him why he thought this might be the case – to which he replied that such a slow-moving and unprotected animal must be easy prey for predators, and poison would thus be an obvious form of protection. I finally understood his question; he had asked it because he was unaware that Acontias is a burrowing creature, escaping predation by hiding underground. If Acontias were to live above ground, it would indeed become easy prey. Thanks to his work and that of his students, we now know that Verreaux’s meadow mouse is an important pollinator of the fynbos plant Protea nana (Biccard and Midgley 2009). Rodents have also been implicated as pollinators of several other fynbos plants (Kleizen et al. 2008; Letten and Midgley 2009), and their role in such rodent–plant interactions, as they are known, has probably been greatly under-appreciated and certainly under-reported. Similar interactions have not yet been documented in other parts of Africa. Marine ecosystems The discerning reader will have noticed that I have omitted one major and extremely important ecosystem from this discussion: the marine ecosystem. 34

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This book is about Africa, and marine ecosystems are an integral part of any continent – thus the marine ecosystem deserves a full airing, particularly since the southern oceans around southern Africa are home to the greatest number of cetacean (whale and dolphin) species on Earth. This is not my area of expertise, and it would be arrogant to claim that I can put them into proper ­perspective. Before I move on, however, I would like to point out some obvious – and some not so obvious – linkages between the marine ecosystem and terrestrial ones. Due to the inherent properties of water, marine environments play an important role in thermo-regulation: the warm Agulhas current that runs southwards down the eastern (Indian Ocean) side of Africa distributes warm moist air into the temperate parts of eastern South Africa; conversely, the frigid Benguela current that runs northward from Antarctica has a cooling and drying effect on the western (Atlantic) side of southern Africa, resulting in a large swathe of desert and semi-arid conditions running from South Africa north to south-western Angola. The impacts of oceans on climate are well known. Perhaps less well known are the impacts of the flow of nutrients between the marine and terrestrial ecosystems. Rivers, of course, carry nutrients and sediments from the continent into the ocean. But nutrients also flow in the opposite direction. Seabirds such as gulls and terns feed almost exclusively on marine life, but move to land to roost and breed. Albatrosses, petrels and shearwaters are more pelagic, but even these species need to return to land to breed, albeit mostly to remote oceanic islands. A mammalian analogue to seabirds is seals. On the Namibian coast, almost 200 kilometres north of the port of Walvis Bay, lies Cape Cross. First ‘discovered’ by Diago Cao in 1488, as the Portuguese pushed southwards along the west coast of Africa – although the indigenous San people had, of course, been hunting along this coastline for centuries – it is now a protected area and home to a colony of several thousand Cape fur seals (Arctocephalus pusillus). With each adult weighing between 60 and 250 kilograms (adult males being four times larger than females, on average), this forms an impressive mammalian standing biomass. A visit to Cape Cross is essential to appreciate the magnitude of this seal colony. There are enough of these seals to support numerous black-backed jackals (Canis mesomelas) that scamper between the marine mammals in search of dead or dying individuals; these jackals, along with other scavengers such as the brown hyena (Hyaena brunnea), are thus beneficiaries of the nutrient-rich upwellings associated with the Benguela current. In this setting seabirds and seals move essential nutrients from the ocean to the land, which enriches terrestrial ecosystems. 35

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*** The African ecosystems I have described in this chapter (see figures 1.6, 1.7, 1.8) are those that exist on a broad geographical scale; they are sometimes known as biomes. However, I have purposefully steered clear of this term because of the many different ways in which ecologists have defined it in the past. Biomes are integrally linked to plants and are therefore less heeded by zoologists than by botanists. A broadly acceptable definition of a biome would probably be something along these lines: a ‘major natural system as determined by its vegetation, general climate and dominant organisms’ (Eichhorn 2020, 4). In this book I will prefer the use of the term ‘ecosystem’. Of course, many more ecosystems exist in Africa than the ones discussed in this chapter – the coastal forests of the eastern seaboard, to name but one – and many that I have lumped into a single description actually comprise multiple finer-grained categories. This chapter has shown us the diversity of Africa’s mammalian community. The continent’s rich biodiversity includes species or groups of species that provide various and valuable ecosystem services. Megafauna such as elephants and hippopotamuses, for example, act as ecosystem engineers, bringing significant change to vegetation and landscape. Bats feed on insects and insect pests, increasing farmers’ harvests and thus their earnings, and saving them money that would otherwise have been spent on insecticides. Animal and plant species and their ecological functions are, however, just one component of biodiversity. Ecosystems, which are built up by collections of interacting species, provide yet another dimension. Throughout this chapter I have referred to ‘species’ as though this is a clearly defined and universally understood concept. But what exactly is a species? In the next chapter, we will see that this is not as simple a question as it may first appear.

36

CHAPTER

2

The Species Conundrum

W

e saw in chapter 1 that Africa plays host to an amazing array of indigenous life forms. More than 1 100 mammal and 2 200 bird species have been recorded on the continent, and although no official count of insect species is yet available, we can be sure that it will number well over 100 000 and that an even greater number remain undiscovered. How do zoologists cope with such a staggering diversity of species? Before we attempt to answer this question, we need to know exactly what we mean by the term ‘species’.

FUNCTION OR FORM? Before considering how we humans make sense of all this bewildering natural variety, it might be instructive to see how other animals go about it. Gorillas (genus Gorilla), as a close relative of ours, provide an interesting example (figure 2.1). These herbivorous great apes seek out specific plants to eat, pursue others for their medicinal value (Huffman 2003), and avoid those that they know to be either poisonous or not sufficiently nutritious to make harvesting them worthwhile. Gorillas, in other words, are ethnobotanists par excellence. They can recognise an exceptionally large variety of plant species. At Bwindi Impenetrable National Park in western Uganda, where gorillas have been studied for decades, botanists have compiled a plant checklist of 1 405 species (Plumptre et al. 2007).

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Figure 2.1. Mountain gorillas (Gorilla beringei beringei ). Photograph by Mike Unwin.

How does a gorilla acquire and manage its knowledge of all these plant species? We don’t know what thought processes go through the great ape’s mind before it plucks a leaf from a shrub, but we can presume it has its own classification system for plants, in which they are categorised according to the functions they perform: this one is edible, this one is poisonous, this one can cure an irritated bowel – and so on. In a similar way, vervet monkeys (Chlorocebus aethiops) take a functional approach to categorising predators. Previous research (Seyfarth et al. 1980) has shown that these sociable primates use different warning vocalisations to distinguish between their three most significant predators: leopards, eagles and snakes. From a vervet monkey’s perspective, this makes perfect sense. These three predators hunt in different ways – eagles swooping from above, leopards stalking through the undergrowth and snakes lurking in the grass – and so each represents a different form of danger. The monkey must be able to communicate this distinction quickly in order that it and its companions can take appropriate evasive action. However, it has no need for finer details about each predator type. As far as vervet monkeys are concerned, three different vocalisations are

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The Species Conundrum

enough to cover the entire spectrum of potential predators. Thus, the ‘eagle’ alarm call will work equally for a martial eagle (Polemaetus bellicosus), crowned eagle (Stephanoaetus coronatus) and several other large predatory raptors, while the ‘snake’ alarm call will serve equally for a South African rock python (Python natalensis), black mamba (Dendroaspis polylepis) and other potentially dangerous snakes. We humans could use the same functional approach to classify life forms. Indeed, non-scientists do this all the time. A householder might use the term ‘creepy-crawlies’ to group organisms from a wide taxonomic spectrum that they would rather not find in their kitchen (spiders, slugs, cockroaches and so on), while a farmer might categorise crows and pigeons, unrelated birds, as ‘vermin’ for the perceived damage they cause to crops. The result of such a classification system would be to create ‘functional species’. These species would be identifiable and distinguishable by their functional properties, and the groups within which we classify them would serve a functional purpose. However, if we were to use this ‘functional species’ concept to classify the diversity of all life around us, we would soon encounter problems. For a start, many (if not most) species have little relevance to humans and therefore play no obvious functional role in our lives. What do we do with these species? Do we simply lump them all together in a group labelled ‘non-functional organisms’? So, if ‘functional species’ is not a satisfactory concept, what other classification approaches could we employ? In fact, there are several other species concepts, each with its own pros and cons. For a start, we could base our identification of a species on some obvious, perhaps external, physical feature. A leopard (Panthera pardus) can be distinguished from a lion (Panthera leo), for example, by its smaller size and spotted coat. This is known as the ‘morphological species’ concept, because it reflects physical form – morphology. It is slightly more satisfying than the functional species concept because we are not organising the diversity of life forms around our subjective human needs. But as it stands, the morphological species concept soon runs into trouble. What do we do with a type of animal that differs considerably in external appearance from another type, but readily breeds or hybridises with it? Lions and tigers would be a case in point. Conversely, what do we do with two types of animal that look alike but do not interbreed, perhaps because of differences in their chromosome numbers?

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Closely related species that are all but indistinguishable from each other by external characteristics are called ‘cryptic species’. These are extremely common – notably among small mammals. An example is the multimammate mouse in the genus Mastomys. In South Africa, it comes in two forms, one that has a diploid chromosome count of 2n = 32 (that is, it has 16 pairs of chromosomes), and another one that has 2n = 36 (18 pairs of chromosomes). These two forms are indistinguishable, even by experts, unless their chromosomes are counted (Venturi et al. 2004). But – and here is the interesting fact – they do not readily interbreed. And even when they are bred, in the artificial conditions of a laboratory, the hybrids do not survive to adulthood and therefore fail to propagate their genes. So, do these two mice represent two forms of one single species? The morphological species concept would tell us that they do, since they share the same physical features and appearance. However, based on the phylogenetic species concept (discussed below), they are two separate species, Mastomys natalensis (2n = 32) and Mastomys coucha (2n = 36). Another problem with the morphological species concept is that the delimitation of a species is based on a subjective value judgement. At what stage is the difference between two types of animal large enough for us to say that they constitute different species? This involves drawing an arbitrary line in a continuum. A small difference may be sufficient for me, but you might object and claim that a larger difference is necessary. And who is to say which one of us is correct? At this point you might object to my handling of the species issue. After all, isn’t every species of animal and plant a single, immutable entity? Hasn’t nature (or, if you prefer, some divine being) created it as such? Why am I confusing the matter by talking about ‘species concepts’: surely each species is uniquely identifiable and distinguishable from every other species on this planet? Well, actually no. And this, in essence, is the whole problem with identifying species: had species been specially created, we would not be struggling to define what a species is. But this book is not the place to discuss creationist theory and other theological issues. As scientists, what we do know is that species change over time, evolving into new species or going extinct. Before we can reach a meaningful definition of what a species is, therefore, we will need to get to grips with how species evolve.

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The Species Conundrum

THE SPECIES PRODUCTION LINE Species come into being via a process known as speciation. The spitting cobra (Naja nigricincta) offers a useful illustration of how this works. This impressive reptile is widespread across the western arid zone of southern Africa, but takes two quite different forms. In the south of its range, from South Africa to central Namibia, it occurs as a jet-black snake and is known as the black spitting cobra (Naja nigricincta woodi) (figure 2.2). In central and northern Namibia, it occurs as a handsome banded snake and is known as the western barred spitting cobra (Naja nigricincta nigricincta). These two forms are easily distinguishable, even by an inexperienced observer. What makes them so interesting is that they overlap in a narrow zone in central Namibia, where they hybridise. What is going on here? How can two such apparently different animals interbreed? Such hybridisation is not rare and occurs in a wide range of species and across the world. Other examples in Africa include the hybridisation between the Livingstone’s turaco (Tauraco livingstonii) and Knysna turaco (Tauraco corythaix)

Figure 2.2. A black spitting cobra (Naja nigricincta woodi ). Photograph by Andrew A. Turner.

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in St Lucia (northern KwaZulu-Natal, South Africa), and that between the hamadryas baboon (Papio hamadryas) and olive baboon (Papio anubis) in east Africa. In fact, hybrid populations have been recorded in scores of mammals, including deer, shrews, a variety of rodents, hares and rabbits, genets and primates (Shurtliff 2013). Hence, finding hybrids in nature is not difficult. Speciation by geographic isolation In a world where species had been fashioned by a creator, hybrid zones might be puzzling. In the context of a world shaped by evolution, however, they make perfect sense. To understand the broad process of speciation, consider the analogy of human accents, dialects and languages. The Australian accent, immediately recognisable anywhere in the English-speaking world, has evolved over just seven or eight generations. The accent of English-speaking South Africans has evolved in a similar period of time. Three hundred years ago English was not spoken in either Australia or southern Africa. How has one language (English) with a clearly defined grammar and lexicon come to change so significantly in such a short period of time? We may not know the specific circumstances that have led to South Africans and Australians pronouncing the greeting ‘Good day’ so differently, but we do know that the introduction of a new language to a geographically isolated region will lead to the development of a unique local accent within the space of just a few generations. The more isolated the location, the quicker the evolution of the local accent will be. Now let us apply that principle to species. Although the processes involved in the development of dialects are different from those of speciation, both are abetted by geographical isolation. Imagine a hypothetical population whose members inhabit a defined geographic area. Suitable habitat occurs throughout this region, allowing individuals of this species to move freely within this area, and individuals from either end of the population may meet and mate. Now imagine a situation where this same population is divided by a topographical barrier such as a mountain, a river, or an ocean. Individuals on one side of the barrier can no longer reach those on the other side, and must thus restrict their mating to their side of the barrier only. In effect, the original population has been split in two. An individual can now contribute its genes only to the subpopulation in which it resides; they will no longer have any impact on the other subpopulation. As a result, these two subpopulations now find themselves

42

The Species Conundrum

on different evolutionary trajectories. Any new genes that might arise by mutation in one subpopulation cannot reach the other. Equally, an allele may randomly disappear from the one subpopulation whereas it may continue to persist in the other one, eventually leading to novel and unique features within each subpopulation.1 Over time, these novel features will distinguish the individuals on one side of the barrier from those on the other; the longer the duration of separation, the greater these differences become. What if the barrier were to disappear? Individuals from either side of the partition would once again be in contact with each other. But would they still be able to recognise each other as potential mates, and therefore contribute genes to each other’s formerly segregated gene pools? If the changes are not too great, and have not impacted on the reproductive biology of the subpopulations, this would be perfectly possible. Such interbreeding would quickly eliminate any differences that might have arisen when the two subpopulations were isolated. On the other hand, should the modifications have created differences too substantial to overcome, such as changes in chromosome number leading to sterility of the offspring, then the two subpopulations would remain reproductively isolated and would no longer share a common gene pool. Thus, one species would have given rise to two. This is what we mean by speciation. In this model of speciation by geographic isolation (known as allopatric speciation), we would generally expect closely related species to be closely associated in space, and to find hybridisation zones between certain subpopulations, where the process of speciation has not reached completion. And indeed, both these expectations are borne out by the evidence. Hybridisation zones abound in nature, and the degree of genetic relatedness between species decreases with increasing distance between them; in other words, closely related species tend to be distributed in similar parts of the world. The Earth’s changing landscape At this point you might argue that geographic barriers do not just emerge out of thin air. Surely the likes of mountain ranges and river valleys are permanent features of our landscape? In fact, this is not the case. Our planet is far from a stable place (see chapter 3). For example, the climate changes predictably from season to season within one year, and less predictably from one year to another. A drought year might be followed by flooding the following year. But the

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climate has also changed more dramatically over much greater time spans. Over the past two million years, the Earth has experienced cold periods (glacials) interrupted by shorter warm periods (interglacials). We are currently sitting, comfortably, in the middle – or perhaps towards the end – of an interglacial that started about 10 000 years ago. Before that, the Earth was gripped by an ice age (glacial) that extended back some 100 000 years. These increases and decreases in temperature and rainfall have profound effects on the landscape. During a glaciation event, ice may cover extensive areas of land, locking up water from the oceans and hence dropping sea levels. The impacts of climate change on African landscapes have been severe. For example, around 20 000 years ago, the Congo Basin was not blanketed in forest, as it is today, but was predominantly a savanna (Maley and Brenac 1998). At about the same time, Lake Victoria, today shared by Kenya, Tanzania and Uganda, was empty of water, and therefore not a lake at all. We will explore the impact of changing climate on the evolution of African mammals in chapter 5. The climate is not the only changeable aspect of our planet. The geological landscape (literally, the ground beneath our feet) is also in a constant state of flux. The crust of the Earth is fractured into about a dozen plates, each moving in relation to its neighbours. These plates are generally forced apart at the midocean ridge system, a chain of mountains that runs throughout all the oceans. At the sides of these plates where ocean meets continent, the oceanic crust is subducted beneath the continental crust. Where two continents meet, neither plate subducts the other. Instead both are pushed up to form mountains. The Himalayas were formed when the Indian plate collided with the European plate, pushing the land upwards. Geological activity may change the structure of the landscape profoundly. Continents may split and become isolated land masses; new mountain ranges may form at the boundary of colliding plates; volcanoes and earthquakes may completely devastate an area; rivers may evolve into deeply incised valleys or change direction and cut a completely new course. We will return to the impact of this activity on the evolution of the African landscape in chapter 5. The point is that a stable environment is not – and never has been – the norm on this planet. Interestingly, it is intermediate levels of instability that create the highest levels of speciation: too much stability and populations are not readily isolated so speciation is curbed; too much instability and populations cannot adapt to local environments and may become extinct. 44

The Species Conundrum

Returning to the example of the cobra, the western barred spitting cobra (Naja nigricincta nigricincta) occurs from the Kuiseb River in Namibia north into south-western Angola. In contrast, the black spitting cobra (Naja nigricincta woodi) occurs south of the Kuiseb all the way into north-western South Africa (Broadley 1974). Where the two forms – currently recognised as subspecies (Wüster et al. 2007) – meet along the Kuiseb River in the dry Namib, they hybridise.2 Although the details of the biogeography of these two subspecies have not yet been determined, it is plausible that they had more restricted – and discrete – ranges in the past, perhaps even during the most recent glacial. We can presume that it was during this period of isolation from each other that the two developed their characteristic and unique features but did not differentiate sufficiently for members of the one form to reject mating with members of the other. With the warmer, wetter conditions of the interglacial period that followed, their ranges may thus have expanded to take on the pattern that we know today.

LINEAGES OF DESCENT Now that we understand how species arise, we can reflect further on a species concept that might be useful to us. A species concept is a human construct, of course, developed to assist us in making sense of the enormous diversity of life by pigeon-holing it into useful but artificial categories. In this sense, perhaps species concepts do not reflect objective biological reality. However, this does not necessarily imply that species (as opposed to species concepts) are not real. Species are real in the sense that they represent indisputable lineages of descent. The one undeniable fact about life is this: every individual organism is necessarily descended from parents (or a single parent), who themselves were descended from parents, and so on, in a continuous, unbroken chain stretching back in time. This chain can never have been broken; otherwise, the individual we are looking at today could never have existed. If your great-grandfather had not existed, neither would you. Each species represents a lineage that is typically distinct from all other lineages. This distinction may come from reproductive isolation from other lineages, or it may be the result of spatial (geographical) isolation. Therefore, if we define species in terms of evolutionarily distinct lineages, we are recognising, and giving import to, the process by which 45

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species are created. This way of identifying species is as natural a way as we can hope for. Such an approach brings practical problems, which may complicate things but are not insurmountable. One such problem is that lineages change as they traverse evolutionary time. We will deal with this in the next section. Another is the difficulty of identifying such evolutionary lineages in the first instance. Organisms do not obviously announce their line of descent. Humans are a partial exception because in our individual identities we carry the name of our paternal (or in some cases, maternal) ancestor. But does an equivalent identifier of familial identity, passed down from generation to generation, exist among other organisms? In fact, it does, and this identifier is the hereditary material present within them. In nearly all organisms, heredity is stored in the molecule known as DNA (deoxyribonucleic acid), although some primitive viruses and bacteria still use RNA (ribonucleic acid). The structure of the DNA molecule (figure 2.3) was unraveled only as recently as 1953. American biologist James Watson and English biophysicist Francis Crick have long received the credit for this game-changing discovery, although the essential contributions of English chemist Rosalind Franklin are not generally known or acknowledged – hardly surprising in the male-dominated field of science. We now know that DNA carries the code that eventually results in the manufacture of an organism, and we know that it is passed on from parents to offspring. All living organisms have DNA (or, in a few exceptions, RNA) that carries the code needed to create proteins, and hence ultimately to construct the very creatures that will replicate the code into the future. The code is ‘written’ into the DNA in the form of sequences of four base pairs, referred to as A, T, G and C, which may run into billions of base pairs for most organisms.3 This code functions to manufacture

G

T

A

C

G

T

G

T

C

A

T

G

C

A

C

A

Figure 2.3. The double helix structure of the DNA molecule. Graphic created by Sandile Motsa.

46

The Species Conundrum

an organism, but it also carries valuable information about the organism’s past – since the code is inherited and passed on from generation to generation. By sequencing relevant sections of an organism’s DNA, we are essentially giving each individual a surname. But we are not confined to just surnames. By sequencing mitochondrial genes, which are inherited by both sexes from just the mother, we are also able to give each individual a maiden name as well. We can then compare these ‘names’ (sequences of DNA) of different individual organisms to determine who shares the same ancestor and who does not. Reconstructing the ancestral relationships of individuals allows us to identify the lineages to which they belong. Lineages change across evolutionary time We can go further than just reconstructing the lineages of organisms. DNA sequences change over time as a result of mutations – random mistakes in the coding process resulting in altered base pairs of the DNA molecule. DNA is passed on to future generations through sex cells, which in all animals, including humans, take the form of sperm and eggs (or ova). In order to produce multiple copies of these sex cells, the DNA molecule needs to divide.4 It does this by unzipping the double helix, with each of the two single strands producing a new complementary mirror image of the DNA molecule. Thus, two double helices are produced from the single double helix. Occasionally an error is introduced during this copying process and the new sex cell ends up with a slightly altered sequence of base pairs. We might liken this to the change of a surname from ‘Whyte’ to ‘White’ due to a typographical error. The importance of mutation to us here is that the altered base pair sequences (see note 3) will not only sort the individuals into different lineages but will also give us an indication of when that split took place. This is because the rate of mutation within a specific population appears to be constant, in effect acting as a ‘molecular clock’. The horseshoe bats provide an interesting example. All horseshoe bats are included in the genus Rhinolophus, the only genus in the family Rhinolophidae (figure 2.4). This monotypic family (that is, a family represented by just one genus) is distributed throughout the Old World and Australia, with more than a hundred species recognised, but until recently scientists had puzzled over the exact relationships within the genus. Furthermore, they were unsure about the provenance of this family: did it

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Figure 2.4. A Rüppell’s horseshoe bat (Rhinolophus fumigatus) from Mozambique. Photograph by Ara Monadjem.

evolve in Africa, or is it of Indomalayan or European extraction? When did the different invasions take place? Samantha Stoffberg and her colleagues recently went a long way towards answering these questions (Stoffberg et al. 2010). By obtaining tissue samples from almost half of the 77 species recognised at the time of their study, they were able to sequence three nuclear genes (inherited from both parents) and one mitochondrial gene (inherited only from the mother).5 They were able to show that the Rhinolophidae diverged from the Hipposideridae, the most closely related family, 40 million years ago, and that the African and Asian clades (phylogenetic groups that are related by a common ancestry) split ‘shortly’ thereafter, at 35 million years ago. Much of the speciation within both these clades took place about 15 million years ago. Their data also suggest an Indomalayan origin for this family, although this is not yet 48

The Species Conundrum

conclusive. Interestingly, these findings from molecular studies mirror those from the study of fossil rhinolophid and hipposiderid bats, suggesting congruence between the genetic and palaeontological methods. The Rhinolophus bats illustrate a relatively slow speciation rate when compared with other small mammals such as rodents. For example, the seven species of grass mice in the genus Arvicanthus of east and north Africa split from the related striped mice in the genus Lemniscomys about six million years ago, and most of the speciation within the former has taken place in the past one to three million years (Abdel Rahman Ahmed et al. 2008). Again, there is close corroboration from the fossil record, giving us extra confidence in the conclusions drawn from this molecular study. Molecular data, therefore, give us a rare opportunity to look back into the past and reconstruct phylogenetic relationships – those developed through evolution – with some degree of confidence. Of course, systematics, the study of evolutionary relationships between different organisms, did not wait for advances in genetic or molecular techniques before it developed. Such phylogenetic reconstructions have been made ever since the time of Charles Darwin. However, the power of molecular techniques to resolve relationships within and between different groups is now widely recognised, especially when they are independently corroborated by the evidence of fossils. A good case in point is our improved understanding of the ordinal (that is, the taxonomic level of the order) relationships among birds. On anatomical grounds, there are many similarities between falcons and hawks, but few between parrots and songbirds (the group that includes finches, warblers and thrushes). Falcons and hawks both have enlarged talons for killing prey and hooked beaks for plucking flesh from the carcass. Not surprisingly, traditional systematists placed these two groups of birds in the same order: Falconiformes. In contrast, there do not appear to be any obvious morphological features shared by a parrot and a thrush, so they were, also not surprisingly, placed in two separate orders: Psittaciformes and Passeriformes. You can imagine the commotion in ornithological circles when, in 2008, a team of 18 scientists published a new ordinal-level phylogeny for birds that placed the parrots alongside the songbirds, with the falcons as a sister group (Hackett et al. 2008). Parrots, songbirds and falcons retain their ordinal names, but the hawks are now in the order Accipitriformes, and literally on the other side of the avian evolutionary tree from the Falconiformes, which are now greatly reduced in diversity. 49

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In fact, this innovation is not as surprising as it might at first have appeared. Molecular techniques had been introduced into the study of bird systematics more than two decades earlier. In a landmark 1990 publication, Charles Sibley and Jon Ahlquist used a technique called DNA-DNA hybridisation to present what they considered to be the true relationships between bird groups (Sibley and Ahlquist 1990). If you have ever wondered why field guides such as the latest Roberts Birds of Southern Africa (Hockey et al. 2005) have completely overturned the traditional order in which bird groups were once presented, the reason is rooted in the work of Sibley and Ahlquist. After perhaps half a century of relative stability, bird systematics, both at higher (ordinal) and lower (species) levels, was plunged into chaos. But out of that chaos a new phylogeny is being forged, one that is hopefully a more accurate reflection of the evolutionary history of this richly diverse class of animals.

WHAT’S IN A NAME? So, we can delimit a species – and thus give it an identity separate from other species – using the concept of an evolutionary lineage. In the previous section, we saw how this has been done at different scales. But delimiting a species and elucidating its closest relatives does not entirely solve our problem of devising a logical classification system that can handle the millions of species populating our planet. To turn our lineages into such a classification system, we need to give these species names. I raised a concern earlier that lineages are, by definition, not static, and therefore species names are meaningless across evolutionary time. What can be done about this? Well, not much. It is something that we just have to accept. Names can be valid at a single point in time; however, we should not try to force these names onto species from a different time – such as fossils from 70 million years ago. As I have explained above, while lineages are real, the names we give these lineages are our own human constructs. Nonetheless, names are indispensable to any biologist. Anyone who has ever opened a field guide will have encountered the binomial naming system, in which every species receives a two-part scientific name derived from Latin and/or Greek, with the first part denoting the genus and the second part the species. The animal we know by the common name ‘lion’, for example, is Panthera leo, with Panthera denoting the ‘big cats’ 50

The Species Conundrum

genus and leo denoting the species. This system was introduced by the celebrated Swedish botanist and zoologist Carl Linnaeus (1707–1778), whose Systemae Naturae, published in its tenth edition in 1758, is considered the starting point of all modern taxonomy. In his works, Linnaeus described some 10 200 species of plant and animal, giving each one a genus and a species name. Linnaeus did more than simply name organisms, however. He also introduced a hierarchical classification system in which taxa at each level were nested within taxa at a higher level (see table 2.1). These taxa were grouped on the basis of perceived similarities. The importance of this system is that it is inherently rich in information. If I were to tell you that I have discovered a species new to science, one never seen by any other human being, you might be curious to know what it is. If I were then to tell you that it doesn’t yet have a species name, but that it belongs to the family Elapidae, you could immediately deduce that it must have no limbs, two eyes and a vomeronasal organ. You would also know that it regulates its body temperature from sources outside its body, that it is missing the loreal scale (between the nasal and preorbital scales), that it is front-fanged, and that it quite possibly has deadly venom. You would know all this, and much more, because of the hierarchical classification system devised by Linnaeus. Elapidae is the family that comprises mambas and cobras. This taxon is, in turn, nested within the higher-level taxon Serpentes (snakes) which itself is nested in Squamata – and so on up the ladder to the kingdom Animalia.6 All Elapidae fall within the Serpentes and all Serpentes within the Squamata. There are no exceptions. We do not find some elapids in

Table 2.1. The taxonomic ranks used in the classification of organisms, using the examples of African elephant, striped mouse, Egyptian slit-faced bat, and leopard. Taxonomic rank

Examples African elephant

Striped mouse

Egyptian slitfaced bat

Leopard

Class

Mammalia

Mammalia

Mammalia

Mammalia

Order

Proboscidea

Rodentia

Chiroptera

Carnivora

Family

Elephantidae

Muridae

Nycteridae

Felidae

Genus

Loxodonta

Lemniscomys

Nycteris

Panthera

Species

africana

rosalia

thebaica

pardus

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the Serpentes and some elapids in a different group, say the Anura (frogs). All members of a taxon share a set of similar features. By assigning an organism to a particular taxon, you are thus, in effect, describing those features. That is why you would know that our mystery species lacked a loreal scale, because all elapids lack that scale. It also explains why, if you were presented with a set of horns that you had never seen before, you would still be able to take a guess that the possessor of those horns was a large, furry, plant-eating mammal that nourishes its offspring (if it is a female) with a special mammary gland secretion that we call milk. This is exactly what faced the discoverers of the saola (Pseudoryx nghetinhensis), a hitherto unknown antelope from the border regions of Laos and Vietnam in South East Asia, when they stumbled across its horns in a Laotian market in 1992 (Robichaud 1998). The other fundamental development that Linnaeus pioneered was to both assign a detailed description and lodge a museum specimen for each new name that was created. With this approach, there could no longer be any doubt as to what species was being referred to. When a herpetologist mentions Arthroleptella rugosa, we know that this refers to a small frog (19 millimetres in length, to be precise) inhabiting the Cape Fold Mountains of South Africa (figure 2.5). We also know exactly what its characteristic features are, because they have been described in a detailed publication by the discoverers of the species, Andrew Turner and Alan Channing (Turner and Channing 2008). And if we are not convinced by their description, we can examine the specimen on which it was based, which – in this case – is housed in the Iziko South African Museum in Cape Town, with the accession number SAM ZR 52094. This first described specimen is called the ‘type specimen’. It represents its species whenever the need arises. The essence of this system is that every name given to an organism can be traced back to a museum or herbarium specimen, allowing for detailed comparisons to be made. This means that, in theory, we will always know what the discoverer of a new organism actually discovered. In practice, this is complicated by the destruction (for example, the fire in the Museu Bocage, Lisbon, which destroyed many type specimens of African bats) or deterioration of specimens. Examination of such type material is critical to the description and naming of new species. Before we name a new species, we first need to ensure that it actually is a new species. Otherwise, we might be (re)describing a species that has already been described, and thus introducing a new name – in 52

The Species Conundrum

Figure 2.5. The rough moss frog (Arthroleptella rugosa). Photograph by Andrew A. Turner.

this case, called a junior synonym – for a species that already has a name. This unwitting and confusing duplication still happens too frequently. It was understandable a century ago, when zoologists from different countries or different regions within the same country often worked in total ignorance of each other. It is less excusable in today’s highly connected and integrated world, however, and is usually the result of sloppy work. Fortunately, taxonomists are as a rule very attentive to detail, and the new philosophy of ‘integrative taxonomy’ brings a greater discipline to the delineation of species and suggests caution when naming a new one (Dayrat 2005; Goodman, Rakotondramanana et al. 2015). Changing names of species You may have been wondering why the scientific names of species change so frequently. For example, I grew up learning about the tree Lonchocarpus capassa 53

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(commonly known as apple-leaf or African rain-tree). This is now known as Philenoptera violacea – a completely different name in both parts. The beautifully illustrated Frogs of Southern Africa (Du Preez and Carruthers 2009) includes 13 new genera that were not there when I first became interested in frogs in the late 1980s. Only one of these represents a genuinely new taxon; the rest are just name changes. What is going on? Are taxonomists just tinkering with names because they have nothing better to do with their time? Sometimes this might appear to be the case, but generally there is a good reason. Of course, some new names do reflect new species previously not known to science in any form. During the 20-year period from 1989 to 2008, for example, 138 totally new species of mammal from Africa were described, including species found in Madagascar and its other associated islands (Hoffmann et al. 2009). One was the horseshoe bat (Rhinolophus sakejiensis), which was described in 2002 by Woody Cotterill based on a series of three specimens captured in northwestern Zambia (Cotterill 2002). This new horseshoe bat is different from all other known horseshoe bats, so its taxonomic status is not in dispute; however, it has not been captured or collected since Cotterill first encountered those three specimens. Indeed, the horseshoe bat family appears to be particularly rich in undescribed species, with a recent study suggesting that up to 12 undescribed cryptic species from tropical Africa alone may lurk in the drawers of museum cabinets (Demos et al. 2019). How many more species may remain completely undiscovered in their tropical havens? Since 2008, I have been involved in the description of more than a dozen new species of bat and one interesting rodent of the genus Colomys.7 However, the undisputed champion ‘new species describer’ of African small mammals is Steve Goodman, who has devoted most of his career to unravelling the systematics of Madagascar’s fauna. During this time, he has described no fewer than 50 new species of bird, mammal, reptile, scorpion and plant, including a tick and a fern. His contributions have not gone unnoticed, and he has received several prestigious awards, the money from which he typically pours back into the organisation he helped to found in 2005, Vahatra.8 He really does epitomise dedication to one’s work. We will meet him again in chapter 4, when we examine the faunas of Africa’s islands. Another reason for introducing new scientific names has to do with our enhanced understanding of the relationships within a particular group. We have already seen how molecular techniques have helped rearrange the ordinal 54

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categories of birds. When we move a particular species of bird from one order (or family) to another, this does not in itself result in a change to the species name. However, when we change the genus, then the species name also changes automatically, since the binomial species name is by definition the genus name plus the species epithet. So, with the aid of new molecular (or occasionally other) insights into the generic relationships of a group of species, we may conclude that a genus includes species very dissimilar from each other; so dissimilar, in fact, that they should be assigned to different genera. When this happens, the species on which the genus was described keeps the genus name, as do all species related to it. All the other species will need a new genus name. *** In this chapter, we have looked at how species are created through the process of speciation, mostly as a result of the geographic isolation of a subpopulation that then diverges genetically along an independent evolutionary pathway. Populations may become isolated from one another by various climatic or geological forces that split them apart. All living organisms have DNA that carries the code needed to construct and replicate them. This code, expressed as a long sequence of four base pairs A, T, G and C, is strung out along the DNA molecule, and carries valuable information about the organism’s past. By sequencing the DNA of different organisms, we can compare their relationship to each other, which allows us to classify and name them. This is what we call taxonomy. It uses a hierarchical system of classification, in which groups are nested within ever larger and more inclusive groups, ensuring that the hierarchy is information-rich from top to bottom. New mammal species are constantly being described, particularly among small mammals such as bats, shrews and rodents. In the next chapter, we will examine the long evolutionary history of mammals, and why southern Africa is such an important place in which to study it.

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CHAPTER

3

The History of Africa’s Mammals

T

he earliest mammal fossils recorded are from the early Jurassic Period almost 200 million years ago.1 But in order to flourish, mammals had to wait for the demise of the dinosaurs. This is believed to have come about 66 million years ago, courtesy of a large asteroid strike on what is now the Yucatán Peninsula in Mexico. In the massive worldwide climate disruption that ensued, at least 75 per cent of plant and animal species on Earth became extinct – including all non-avian dinosaurs. This mass extinction ushered in what is traditionally known, somewhat melodramatically, as ‘The Age of Mammals’.2 With dinosaurs gone, mammals diversified on land, in the water and in the air, growing within 20 million years from species the size of a large rat to giants standing head and shoulders above the largest elephant alive today. Rodents grew to the size of rhinoceroses, and various groups of elephant- and rhinoceros-like quadrupeds regularly topped the scales at well over ten tons; the largest land mammals included Indricotherium transouralicum, a hornless rhinoceros-like creature from Eurasia, and several species of Deinotherium (relatives of the elephant; see figure 3.1) in Eurasia and Africa (Smith et al. 2010). We can thus conclude that it was dinosaurs, a group that included the largest animals that ever walked on land, which limited the diversification of mammals. The dinosaurs forced them to the fringes of existence, where they lived mostly

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Figure 3.1. A Deinotherium. Drawing by Mike Unwin.

as small, furry, scurrying insectivorous creatures, evading the teeth and claws of dinosaurs by seeking shelter in burrows and embracing a nocturnal lifestyle. For this reason, the ancestry of mammals is often depicted as rather unremarkable, overshadowed by the dinosaurs. This chapter aims to convince you otherwise. Mammals have a deep and interesting past, and Africa may well be the best place on Earth in which to study it.

THERAPSIDS: EARLIEST ANCESTORS OF MAMMALS In Africa, the ancestry of mammals is relatively well documented, thanks to rich fossil deposits in the Karoo rocks of central South Africa, and can be traced

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Table 3.1. Geological eras, periods and epochs as relevant to the story of mammals. The beginning of each era (in millions of years ago – mya) is also given. Era

Period

Epoch

Cenozoic

Quaternary

Holocene

Mya

Pleistocene Neogene

Pliocene Miocene

Palaeogene

Oligocene Eocene Palaeocene

Mesozoic

66

Cretaceous Jurassic Triassic

Palaeozoic

252

Permian Carboniferous Devonian Silurian Ordovician Cambrian

541

back some 300 million years to the earliest synapsids. (Table 3.1 lists the geological eras, periods and epochs relevant to the story of mammals). These early synapsids are collectively called pelycosaurs, and include the well-known Dimetrodon, the creature with an impressive dorsal sail that graces many children’s books on dinosaurs, even though it is not one. The sauropsids, a sister group to the synapsids, gave rise to the dinosaurs (a clade that includes birds) and to all modern groups of reptiles, including the turtles and tortoises. By contrast, an advanced group of synapsids, the therapsids, directly gave rise to the mammals. The therapsids were an interesting and diverse group of animals that flourished in the lead-up to, and after, the Permian mass extinction of about 250 million years ago – the cause of which is still not resolved but may have involved a super-volcano and/or a meteor strike. These small- to mediumsized reptiles dominated life on Earth for many millions of years, and included 58

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both vegetarians and carnivores. In fact, more than 500 genera of therapsids have been described, which is a truly staggering diversity, surpassing that of the dinosaurs that followed them. Lystrosaurus is an example of a typical therapsid that lived in southern Africa, apparently in some abundance because its bones dominate certain Karoo rock beds. It was the size of a pig, and had a horny beak and just two teeth – one downward-pointing canine on each side of the upper jaw. In fact, so numerous are the bones of this animal that the geological stratum in which they occur has been named after it: the Lystrosaurus Assemblage Zone (LAZ). The LAZ forms part of the Beaufort Group, which is itself part of the Karoo Supergroup.3 This last stratum is (or should be!) of great interest to mammalogists because its rocks contain fossil ancestors whose existence spanned some 120 million years of mammalian evolution. The Karoo Supergroup underlies all of Lesotho and two-thirds of South Africa, including practically all of the Free State, Eastern Cape and KwaZulu-Natal provinces. However, what we now know as southern Africa had a quite different geography some 330 million years ago, when the first sediments that eventually formed the rocks of this Supergroup were being deposited. Today, central South Africa lies 1 000 metres (or more) above sea level, but during that earlier period this entire area was a shallow sea. Sediments flowed into this sea, forming discrete layers that over geological time, under pressure from layers above, formed the sedimentary rocks we see today (McCarthy and Rubridge 2005). Two things make the Karoo Supergroup of interest to us. First, the sedimentary layers were laid down at a time when the therapsids were first evolving. Second, this deposition continued over the entire span of early mammalian evolution, neatly documenting each stage – and often in surprising detail. Returning to our Lystrosaurus story, the LAZ covers a narrow geographical zone, on average perhaps no more than 50 kilometres wide, forming a ring around Lesotho and an equal-sized chunk of the Eastern Cape to the south (Modesto and Botha-Brink 2010). Within this restricted zone, and in the corresponding geological stratum, the bones of Lystrosaurus may account for up to 95 per cent of all vertebrate remains, suggesting that this genus truly dominated the landscape during this period. All half-dozen species of Lystrosaurus were herbivores, ranging in size from cat to pig. They were toothless, except for the two tusks mentioned earlier, and must have eaten their plant foods using their horny beaks – probably much in the way that tortoises 59

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do (see figure 3.2). Their gait was lizard-like, with their limbs extended sideways, as opposed to mammal-like, where the limbs are aligned directly beneath the body – which lifts the animal higher off the ground and allows for faster motion. Interestingly, the echidnas of modern-day Australia, which belong to a ‘primitive’ group of egg-laying mammals called monotremes, share a similar sprawling gait to that of synapsids (Regnault and Pierce 2018). I mention Lystrosaurus to illustrate an important point about the history of life on our planet. For a lineage to exist through geological time (that is, for more than tens of millions of years), it will at some point need to face and survive a mass extinction event. This is exactly what Lystrosaurus did 250 million years ago, and it came through with flying colours. The end-Permian mass extinction was the deadliest and most comprehensive of them all, killing perhaps 96 per cent of all species in existence at the time. But not Lystrosaurus, which somehow managed to pull through. Its secret? This resourceful animal was a burrower, using its strong forelimbs to dig into the ground. It is thought that by retreating into underground chambers, Lystrosaurus was able to avoid the worst of the atmospheric disruptions created at that time. Indeed, resting up in a burrow is still considered a typical characteristic of many mammals, particularly small ones such as rodents. And Lystrosaurus possessed one

Figure 3.2. A Lystrosaurus. Drawing by Mike Unwin.

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additional feature thought important for its survival: its growth to adulthood was rapid (Botha-Brink and Angielczyk 2010). Rapid growth rate translates into rapid attainment of sexual maturity, which means faster breeding and thus higher levels of abundance than among creatures with lower growth rates. Furthermore, vulnerable youngsters become adults sooner, which allows them to learn to evade predators more quickly. This extraordinarily successful group not only made it through the end-Permian mass extinction but, via adaptive radiation, went on to dominate terrestrial landscapes for several million years.

CYNODONTS: THE NEXT STAGE Eventually Lystrosaurus became extinct. It was not this genus that was the direct ancestor of the later mammals, therefore, but its cousins, the cynodont therapsids. No doubt some cynodonts shared the Lystrosaurus burrowing habit – at least the occupation of burrows, if not the actual digging of them – and the rapid growth of juveniles to adults. Cynodonts first appear in the fossil record at about the same time as Lystrosaurus, in the late Permian Period. They survived the mass extinction and then diversified rapidly to fill many of the terrestrial niches available in the Triassic Period, giving rise to the mammals of the early Jurassic Period (Ruta et al. 2013). Many of the features that we typically associate with modern mammals first evolved in these cynodonts. These features include: differentiated teeth, which allow for a diversification in diet; fur, which is associated with endothermy – the ability of an animal to maintain its body temperature through metabolic processes; and an erect gait, enabled by an evolutionary shift of the limbs from a lateral position to one below the body, which confers greater speed of movement. Parental care, another feature associated with mammals – and shared with birds, but not typically with modern reptiles – has an earlier history, first appearing in the pelycosaurs that I mentioned earlier (Botha-Brink and Modesto 2007). What then, we may ask, separates a cynodont ‘reptile’ from a mammal? Can we pinpoint a stage in time when the creatures we are looking at have crossed the cynodont-to-mammal ‘gap’? In fact, this is not a helpful question – for the simple reason that life survives through time by genealogy (the production of progeny). Hence, the ‘first’ mammal would have had an unbroken 61

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line of descent reaching back to the ancestral cynodont. Any ‘gap’, as Richard Dawkins elegantly explains in The Ancestor’s Tale (Dawkins 2004), appears simply as a by-product of the disappearance of the intermediaries. Mammals today look different from reptiles because the entire line of cynodont descendants by which they were once connected is extinct. However, seeking such distinctions – for example, identifying what differentiates reptiles from mammals – serves a practical purpose by allowing us to arrange the components of today’s living world into helpful categories, even if these categories may be somewhat questionable when viewed within a broader time frame. And there is good reason for doing so, just as long as we remember that such categories are a human construct created to assist our studies, and not an immutable reflection of the natural world and its evolutionary history, as I discussed in chapter 2. Bearing the above in mind, we can say that the only technically watertight distinction between a reptile (including a cynodont therapsid) and a mammal lies in the articulation of the jaw. This may surprise those who remember their biology teachers talking about cold-blooded, egg-laying reptiles as opposed to warm-blooded mammals that give birth to little replicas of themselves. However, the traditional classroom distinction is not particularly useful to evolutionary biologists, because it cannot be applied, or can only be applied with great difficulty, to extinct forms, which make up a large proportion of all the reptiles and mammals that have ever existed on this planet. And, of course, if we want to understand the evolution of reptiles and mammals, we will need to examine the fossil record. A definition that serves only extant species cannot be generalised to all reptiles or all mammals, which is why distinguishing between these two groups based on warm-bloodedness and/ or the laying of eggs becomes impractical. And even today, in fact, those distinctions do not entirely hold true. Not all mammals are warm-blooded, and a few reptiles are at least partially warm-blooded. The leatherback turtle (Dermochelys coriacea), for example, is a reptile with a capacity for endothermy: it can generate and maintain its own body heat in order to survive cold temperatures in the ocean depths (Davenport et al. 1990). In contrast, the naked mole-rat (Heterocephalus glaber) is a mammal that lacks the capacity for endothermy: its body temperature fluctuates with the ambient temperature of its surroundings (Woodley and Buffenstein 2002). Furthermore, not all reptiles lay eggs – many species give birth to live young, and sea snakes of the 62

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subfamily Hydrophiinae even have a placenta (although this feature evolved independently of the mammalian one). Conversely, the Monotremata – an order of primitive mammals that are today confined to Australasia and comprise the platypus (Ornithorhynchus anatinus) and three species of echidna (Tachyglossidae) – do lay eggs. We humans enjoy being warm-blooded. As a mammal that carefully maintains a constant or near-constant core body temperature, we naturally take the view that any fellow mammal incapable of this feat must be disadvantaged. However, maintaining a constant body temperature through metabolic processes is energetically demanding. It may severely challenge the body, especially when food supply – the fuel that stokes the metabolism – is low or unpredictable. We now know that many species of mammal can allow their body temperature to fluctuate, either on a circadian basis or for extended seasonal intervals, in order to reduce energy expenditure.4 Andrew McKechnie, the established star of ecophysiology research in the southern African region, and his lab at the University of Pretoria, have been investigating these processes in birds and bats for the past two decades. Working with a former MSc student, Dawn Toussaint, he demonstrated that the body temperature of Roberts’ flat-headed bat (Sauromys petrophilus), a member of the free-tailed bat family Molossidae, of which some species roost in large numbers in the roofs of houses throughout Africa, varied with air temperature (Toussaint and McKechnie 2012). As the day – and hence the roost in a rock crevice – got hotter, the bats’ body temperature increased, reaching in one individual an incredible 46.5°C. These significant daily fluctuations in body temperature are presumably an effort to reduce evaporative water loss or sweating, which is how most mammals prevent themselves from overheating. As a result, these bats do not need to waste precious water in order to keep their body temperatures from rising. Working with another molossid, the Egyptian free-tailed bat (Tadarida aegyptiaca, figure 3.3), they further demonstrated that bats can also reduce their body temperature, a process that can extend over a prolonged period of several days (Toussaint et al. 2010). During mid-winter, these bats, which were roosting in buildings, allowed their body temperature to drop – in some cases to below 10°C – as night-time temperatures dropped, then allowed them to rise again as temperatures rose during the day. However, when a cold front hit, and roost temperatures fell to around 10°C even during the day, the bats remained 63

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Figure 3.3. An Egyptian free-tailed bat (Tadarida aegyptiaca). Photograph by Lindy Lumsden.

cold for several days in a row, allowing for a drop in their basal metabolic rate, hence reducing their nutritional requirements; this drop in metabolism could be the difference between life and death during such periods of inclement weather, especially for a small-sized mammal. These observations have been advanced as an example of true hibernation in a subtropical bat. However, they are not confined to one or two oddball species. Working with Nomakwezi Mzilikazi, who is now the director of the prestigious National Research Foundation of South Africa, McKechnie reviewed heterothermy in African mammals and showed that it has been reported in 40 species across 6 orders, including the elephant-shrews, rodents, shrews, bats and primates (McKechnie and Mzilikazi 2011). So, we should return to our original question: what distinguishes reptiles from mammals? The difference lies in the way that the jaws are articulated, which in mammals is between the dentary bone of the lower jaw and the squamosal bone of the upper jaw. In reptiles, jaw articulation is performed by the articular and quadrate bones respectively, which in mammals have been relieved of such duties and seconded to the middle ear, making up two of the 64

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three mammalian ear ossicles. This brings us back to why the Karoo geology has been so important for the understanding of mammal evolution: these sedimentary rocks have yielded cynodont fossils with every conceivable combination of jaw articulation, from articular-quadrate to dentary-squamosal. There may be many gaps in the fossil record, but not here!

MULTITUBERCULATA: ALL IN THE TEETH The next chapter in the history of mammals is a long one, extending through the Jurassic and Cretaceous periods, and covering the peak of the ‘Age of Reptiles’. For the first 150 million years or so of their history – which is, of course, our history too – mammals survived as a type of underdog to the larger and more ferocious dinosaurs. Mammals fell prey to carnivorous dinosaurs and were outcompeted by the giant herbivorous sauropods. Hence, mammals remained small and nocturnal, and hid in burrows during the day, their diet consisting of whatever was overlooked or squandered by the dinosaurs. This, at least, is the traditional view offered by most writings on the subject, and it may well be true in broad outline. However, once we investigate the story in more detail, we find that its characters are not quite as stereotyped as we have been led to believe. Certainly, mammals remained small and probably unobtrusive (as most smalland medium-sized mammals remain today – how often do you get good views of a field mouse or a genet?) but within this constraint they carved out a wide variety of lifestyles, diversifying to fill numerous unique ecological roles. A great example of this ‘hidden’ diversification within a group of mammals is that of the multituberculates (order Multituberculata). This group may well be the most successful mammalian order of all time, having survived for 120 million years and diversified into at least 200 known species and 80 genera, yet how many people have ever heard of them? They emerged some 150 million years ago, survived the meteor strike that brought down the curtain on the Cretaceous Period 66 million years ago, and finally went extinct about 31 million years later, without leaving any descendants. I mention the multituberculates here to highlight their rather amazing adaptive radiation before the end-Cretaceous mass extinction. In other words, they diversified into multiple species while the dinosaurs were still around. These primitive mammals, so named because of the multiple tubercles or protuberances 65

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on their cheek teeth, were rodent-like in anatomy and appearance, and probably in behaviour too. Like rodents, they had chisel-like incisors, separated by a gap or diastema from the cheek teeth. Like rodents, they varied in size from that of a mouse to that of a cane-rat. Granted, this is not a spectacular size range compared with that of dinosaurs, which varied from rodent-sized species to giant sauropods the size of a truck. However, here is the key point: these mammals increased in both their body size and the variation in their size (that is, the difference between the largest and smallest species) over the 20-millionyear period leading up to the end-Cretaceous event, despite the presence of the dinosaurs. The first multituberculates weighed 10–100 grams, but by the end of the Cretaceous the largest species weighed in at more than 5 kilograms – a 50-fold increase! Perhaps the biggest surprise with the multituberculates, however, lies in the diversification of their diets – as ascertained by the study of their dentition (Wilson et al. 2012). For almost 60 million years, the cheek teeth of the multituberculates remained simple, indicative of a carnivorous (and animaldominated omnivorous) diet. Next came a period of diversification, during which their teeth became more complex. This complexity is measured by the number and shape of cusps and other protuberances on the teeth. Simple, blade-shaped teeth allow for the shearing of meat. More complex teeth allow for the processing of plant material by providing an occlusal surface: in other words, the cusps on the teeth of the lower jaw grind against those on the corresponding teeth of the upper jaw. It may appear counter-intuitive, but a herbivorous diet demands more complex dentition than a carnivorous one, due to the fibrous nature of vegetation and the fact that plant cell walls are virtually indestructible. What was the spur to this diversification in the multituberculates? Presumably, it had something to do with their diet – as evidenced by the increase in complexity of their teeth. In a 2012 study, Gregory Wilson and his co-authors (Wilson et al. 2012) demonstrated a neat correspondence between, on the one hand, the appearance of angiosperms or flowering plants (which account for the bulk of plant species today) and, on the other, the diversification of the multituberculates. So, it seems that as this new food source appeared in the landscape, the multituberculates were swift to exploit it. The multituberculate story thus serves to remind us that simple broad-scale narratives, such as the supposed lack of mammalian diversity during the time of the dinosaurs, 66

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may overlook key details that might improve our understanding of early mammalian evolution. We now know that a lot was going on during the Cretaceous Period, tens of millions of years before the demise of the dinosaurs. Indeed, so rapid and extensive were the diversifications of insects, squamates, birds and mammals into new taxa during this period that it has been called the ‘Cretaceous Terrestrial Revolution’ (Schipper et al. 2008).5 Undoubtedly, this burst of diversification is directly linked to the arrival of the angiosperms that exploded onto the scene at this time, replacing ferns and gymnosperms – such as pines and cycads – that had predominated for at least 100 million years before the new kids on the block arrived (Barba-Montoya et al. 2018). These new plant communities provided novel sources of food for animals to exploit and new niches for them to occupy. They also enabled new forms of interaction, such as those between plants and their pollinators, which resulted in plenty of interdependence. This was an opportunity that mammals exploited long before the dinosaurs went extinct (Meredith et al. 2011). Interestingly, dinosaurs do not appear to have been part of this process; their diversification rates were, in fact, lower during this period than in the earlier Jurassic Period. The upshot of the Cretaceous Terrestrial Revolution is that from this moment onward, the diversity of life on land overtook that in aquatic environments.6 Today, rough estimates suggest that species richness on land is perhaps four or five times that in marine and freshwater habitats, mostly as a result of the diversity of insects and spiders (Schipper et al. 2008).

AFROTHERIA: AFRICA’S NATIVE MAMMALS What exactly are the original mammals of Africa? Or, put in a different way, which mammalian groups are truly African in the sense that they spent the better part of their evolutionary history in Africa? In some respects, this is a nonsensical question because ‘Africa’ itself has only existed for some 90 million years or so in a way that is recognisable to us today. Thanks to plate tectonics (sometimes, incorrectly, referred to as continental drift), the landmasses that we refer to as continents have not been in their current configuration for long. Our reptilian-like forerunners, the therapsids, inhabited a completely different geographical world from ours, in which the continents were grouped in a single 67

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landmass called Pangaea. At the time that mammals were first evolving, some 200 million years ago, Pangaea had cleaved into a northern landmass called Laurasia and a southern one known as Gondwana. By the time the multituberculates hit the scene some 50 million years later, Gondwana was beginning to split up into the landmasses we now know as South America, Africa, Madagascar, India, Australia and Antarctica (figure 3.4). When the meteor that wiped out

Pangea

Gondwana

Laurasia

Figure 3.4. Map of plate tectonics showing the outline of continents over the past several hundred million years (from Pangaea to the present). Drawing by Mike Unwin.

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the dinosaurs struck some 66 million years ago, the continents were starting to align themselves in an arrangement that we would recognise today, particularly with regard to Africa. But there were still some striking differences: North America was still connected to Eurasia, for example, while Antarctica was still linked, albeit tenuously, to South America on the one hand and Australia on the other. So, to speak of native African mammals requires us to address specifically those mammals that arose 90 million years ago or later. Earlier than this, there simply was no Africa to speak of! Advances in molecular techniques have made it possible to resolve the relationships between previously obscure taxa. For example, scientists long ago realised that elephants, manatees and hyraxes (dassies) were each other’s closest relatives – although ‘closest’ in this case bears little connection to ‘close’, given the extent to which these groups have diverged since they split from one other around 55 million years ago. To this modest collection, genetic sequencing now allows us to add a few more groups: aardvarks, elephant-shrews (for which the alternative name sengi is perhaps less confusing, since they are neither elephants nor shrews), African golden moles and tenrecs. On the face of it, these structurally diverse taxa – now united under the clade name of Afrotheria – do not appear to bear any resemblance to each other, although there is a suggestion of a trunk or extended snout in some of them.7 Without molecular data, the idea of Afrotheria would disintegrate, the anatomical features of its members not being enough to hold them together in our minds. This explains why, when the concept of the Afrotheria was first mooted in the late 1990s, it was met by a bewildered, and in some quarters, sceptical, scientific community. However, the monophyletic nature of this clade is indisputable, as study after study has repeatedly demonstrated (Meredith et al. 2011; Murata et al. 2003; Springer et al. 1997; Stanhope et al. 1998). The Afrotheria also share one other vital characteristic, and it is the one that gives them their name. These very different-looking but closely related groups all evolved together on the same continent. All have spent the past 90 million years in more or less total isolation in Africa. These, then, are Africa’s true ‘native’ mammals. So, what of the other mammals currently occurring in Africa? Are, for example, the carnivores (lions, hyenas and jackals), odd-toed ungulates (rhinoceroses and zebras) and even-toed ungulates (giraffes, pigs and antelopes) ‘African’? These are, after all, iconic creatures that everyone 69

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readily associates with this continent, so we could be excused for believing that they are just as African as the Afrotheria. We would be wrong, however. All these other mammal groups (and many others, including the bats, rodents and primates), evolved on the northern landmass of Laurasia. It was from here that they colonised Africa, presumably either during one of the brief periods of landmass connection or by rafting across the Tethys Sea.8 The bulk of their evolutionary history was played out, not in Africa, but in Eurasia. In contemporary parlance, these might thus be described as ‘alien invasive’ species, when viewed in the longer evolutionary, rather than ecological, time frame. You may be wondering whether this implies that Africa was poor in mammalian biodiversity before the arrival of these ‘recent’ colonists. After all, elephants, hyraxes and aardvarks do not make for a rich assemblage, compared with the prolific variety of antelope, rodents and bats inhabiting Africa today. If so, the answer would be no. The Afrotheria may not include many species alive today, but had we counted their numbers, say, 30 million years ago, we would have reached a totally different conclusion. Take the modern hyraxes (family Procaviidae), which currently include six species in three genera. Hyraxes are small (2–4-kilogram), herbivorous mammals; two genera, Heterohyrax (figure 3.5) and Procavia, are associated with rocky outcrops, and one genus, Dendrohyrax, with large trees within forests. Procavia feeds entirely on grass, evading predators and reducing competition with other grazers by restricting its movements to the vicinity of its rocky strongholds. Heterohyrax is a browser, but essentially exhibits a similar behaviour to Procavia. Dendrohyrax has a more varied diet of foliage, fruit and bark, perhaps as a result of its forest-dwelling nature. Although individual species are widespread and, in places, abundant, the diversity across the hyrax group is, at best, modest. It hardly compares with the diversity of, for example, the 31 genera of the buffalo/antelope family Bovidae that occur in Africa, which comprise 76 species, more or less, and range in size from the diminutive 2.2-kilogram royal antelope (Neotragus pygmaeus) to the enormous 800-kilogram giant eland (Taurotragus derbianus). If we were able to travel back in time, however, we would encounter an impressive array of hyraxes and hyrax-related forms (some 21 genera in total). These included small and structurally similar kinds to modern hyraxes, and others that were larger and ecologically comparable to modern ungulates in their cursorial, plainsliving lifestyle. 70

The History of Africa’s Mammals

Figure 3.5. A yellow-spotted hyrax (Heterohyrax brucei ). Photograph by Ara Monadjem.

In fact, the hyracoids – as this more inclusive group is known – were the dominant small- and medium-sized grazers and browsers of Africa for a period extending over at least 20 million years. It was the adaptive radiation of the African antelopes, starting 25 million years ago, that ecologically marginalised the hyracoids and resulted in the extinction of all but the three extant genera. Hence, this is a tale of diversification, domination and ultimately the extinction of a group. And it would be a sad story were it an exceptional or one-off occurrence. But it is not rare at all. In fact, this process is the norm for life on our planet. Species come and go; groups diversify as environments change, and they sometimes come to dominate a particular ecosystem. In the end, however, these species are replaced by other species or species-groups. Over shorter geological periods this may play out as species substitutions in space, as one species expands its range at the expense of another. Over longer periods, it inevitably results in the complete elimination of species. As a result, Africa’s native mammals have mostly been relegated to the dustbin of extinction. Yet we can hardly bemoan this loss as having scarred life on this continent. We saw, in chapter 1, that African mammalian diversity is high and, in many ways, unique. 71

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FIRST MAMMAL INVASIONS: THE COLONISATION OF AFRICA So, how exactly did the carnivores, ungulates, rodents and bats that all evolved on the northern landmass Laurasia find their way to Africa? Remember that by 90 million years ago, Africa was isolated, effectively surrounded by a moat of oceanic proportions. Any terrestrial animals entering Africa would have had to somehow cross that challenging water barrier. Although Africa was part of the southern landmass of Gondwana, there appears to have been little interchange of terrestrial animals between Africa and the remaining part of Gondwana. In fact, there is no evidence of any mammals having crossed from South America, Madagascar or Australia to Africa. There were, however, several ‘Out of Africa’ events, included those that seeded mammals on Madagascar (see chapter 4) and the stem group of caviomorph rodents and platyrrhine monkeys in South America (Gheerbrant and Rage 2006).9 Despite its Gondwanan roots, once Africa became isolated, its main trading partner with respect to terrestrial mammals (and reptiles) became Laurasia. For about 75 million years, the Tethys Sea remained a formidable barrier to dispersal between Africa and Laurasia, and it was during this period that the native Afrotherians, described above, diversified. Several rodent groups were indeed successful in making this crossing, including the ancestors of the anomalurids (African ‘flying squirrels’) and nesomyids (pouched mice and relatives – see chapter 8), but these were extremely rare events and account for only a handful of colonisations. However, from about 25 million years ago (the exact date is still disputed), after the African plate collided with that of Eurasia (Laurasia itself splitting into Eurasia in the east and North America to the west), increased opportunities arose for the interchange of mammalian faunas. It was during this period that multiple such movements took place, including the colonisation of Africa by the ancestor of the antelopes. We still do not fully understand how terrestrial animals crossed this oceanic barrier. Even a distance of 10 kilometres presents a forbidding challenge to a mammal adapted to living in non-marine habitats, let alone 100 kilometres or more of open ocean. One way is by rafting – using logs, trees and other floating debris to travel, by chance, from the shores of one continent to those of another. Such sweepstake dispersal, as it is called, is hardly a likely scenario, but that does not mean that it could not have happened. In fact, evidently it did happen! When you have hundreds of thousands or millions of years to play with, such 72

The History of Africa’s Mammals

extreme odds become far more plausible. Another important way to improve these odds is by breaking up one long journey into a few smaller ones. For example, islands along the way could act as stepping stones, allowing for shorter individual dispersal events. With the rising and falling of sea levels over time, according to climatic fluctuations, islands may disappear under water or emerge above it, creating and removing such stepping stones. Indeed, the dispersal, in both directions, of multiple species of mammals across the Tethys Sea around 22–23 million years ago aligns neatly with a glaciation event (see chapter 5), during which sea levels would have dropped significantly and exposed just such stepping-stone islands. An even better means of facilitating dispersal between continents is the formation of a physical corridor. Although the coastlines of what we now call Spain and north-west Africa have been separated by a deep sea channel during this entire period, a complete land bridge formed on the eastern flank of north Africa, connecting Africa to Eurasia via Arabia. Thus, while a mammal in the west would have required a sea crossing to disperse from Eurasia to Africa (or vice versa), in the east it could, in theory, have walked across dry land. However, this Arabian land crossing was no stroll in the park. The region was hyperarid when the first major interchanges of mammals were taking place between Eurasia and Africa, and has remained arid to this day, representing a barrier almost as severe – or perhaps even more so – for forest-adapted, water-loving species. Such corridors are typically called ‘filter bridges’ because they act as a filter, only allowing species that have the requisite adaptations – in this case, to hyper-aridity – to get across. In summary, then, the history of mammalian interchange between Africa and Eurasia is roughly as follows (table 3.2). From around 90 million years ago, the earliest native African mammals, the Afrotherians, evolved in situ. They remained the dominant (and only) mammals in Africa for at least 30 million years. Around 60 million years ago, the first mammals arrived from elsewhere, including primitive insectivores and primates. These were followed through the Eocene Epoch (66–23 million years ago) by several separate invasions, including that of the Hyaenadontidae, a type of creodont carnivore closely related to today’s carnivores, and several groups of early rodents. However, the greatest number of exchanges took place during the Miocene Epoch (23–5.3 million years ago), when many groups crossed between Africa and Eurasia (see table 3.2 for examples). 73

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Table 3.2. Some of the mammalian interchanges between Africa and Eurasia over the past 60 million years. Millions of years ago (mya)

Geological epoch

Mammalian group

From Eurasia into Africa

60 mya

Palaeocene

Earliest nonAfrotherian mammals, including insectivores and primates

×

55 mya

Eocene

Leporidae (rabbits and hares)

×

48 mya

Eocene

Zegdoumyid rodents (possible ancestor of Anomaluridae and Pedetidae)

×

42 mya

Eocene

Platyrrhine primates

36 mya

Eocene

Hystricognath rodents, HyenadotCreadonts

×

27 mya

Oligocene

Nesomyid rodents

×

23 mya

Miocene

Early Gerbilline rodents

×

22 mya

Miocene

Tragulids, antelopines, rhinoceroses

×

18–15 mya

Miocene

Shrews, ancestral pigs and giraffids, felids, viverrids, pangolins

×

18–15 mya

Miocene

Elephantids, porcupines, primates, ancestral caprines

14.5 mya

Miocene

Ancestral tragelaphines

From Africa into Eurasia

×

×

×

(Continued ) 74

The History of Africa’s Mammals

Millions of years ago (mya)

Geological epoch

Mammalian group

From Eurasia into Africa

11 mya

Miocene

Murine rodents

×

8 mya

Miocene

Canids

×

6.5 mya

Miocene

Hippopotamids

5 mya

Pliocene

Suine pigs

5 mya

Pliocene

Macaque primates

From Africa into Eurasia

× × ×

Source: Modified from Kingdon et al. (2013).

MODERN INVASIONS: ‘ALIEN’ SPECIES What lessons, if any, can we learn from Africa’s evolutionary past in relation to our treatment of what we call ‘alien invasive’ plants and animals today? What exactly is an alien species? What should we do about the constant stream of organisms colonising new regions? Should we be labelling these species as invasives and treating them differently to indigenous species by planning to eradicate them? These are tricky questions – and I should start by pointing out that I am not in any way implying that the effort and funding devoted to the research and management of alien invasives is misplaced. On the contrary; many of these species have enormous financial and ecological costs associated with them. My point is only that we should think carefully when using terms such as ‘alien’, because in the long term (over geological time) all species are alien. No species is born into a specific geographical range where it dutifully completes its biological activities until it becomes extinct (Thompson 2015). The term ‘alien invasive’ ­typically refers to species that have been moved by the hands (or feet, or vehicles) of humans: for example, the introduction of camels, pigs, rabbits and cats to Australia, all of which have since established feral populations – that is, thriving in the wild in the absence of, or often despite, human intervention. But what do we make of species that have expanded or contracted their ranges due to radical changes in rainfall and/or temperature as a result of human-induced climate change? Have we humans not altered the climate and the physical landscape by the workings of our factories, farming practices and urban developments? 75

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Therefore, can we not say that the species that have expanded their range as a result – and thus, by definition, colonised new geographical areas – have done so by our hand? In southern Africa, for example, the Egyptian goose (Alopochen aegyptiaca), black sparrowhawk (Accipiter melanoleucus) and hadeda ibis (Bostrychia hagedash) have all expanded their range across thousands of square kilometres thanks to changing land use practices, possibly at the expense of native species. We are also seeing changes in the distribution of mammals with, for example, the oribi (Ourebia ourebi, figure 3.6) gradually disappearing from the southern margins of its geographical range in South Africa. Do we invest

Figure 3.6. Oribi (Ourebia ourebi) in Murchison Falls National Park, Uganda. Photograph by Mike Unwin.

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time and effort in eradicating the hadeda ibis from the Western Cape Province of South Africa? Conversely, do we invest in maintaining potentially non-viable populations of oribi in South Africa and Eswatini? I do not pretend to have answers to these questions; I can only reiterate that they are difficult, even possibly intractable, and need proper airing before any useful consensus can be reached. We must remember, however, that although Africa has been the constant recipient of Eurasian mammals over the span of 90 million years, such colonisation events would have been rare and typically taken place at great intervals – probably measured in millions of years. Today, we are assisting organisms to achieve colonisation rates thousands of times greater, and possibly even more than that. Furthermore, the successful arrival on a new landmass of a species with novel ecological skills generally results in local turmoil, as some native species adapt or disappear because of being eaten or competitively nudged aside by the colonist, while others, in turn, find greater opportunities. Hence the composition of communities is changed, and ecosystems are rearranged, while nature adapts over evolutionary time. Of course, colonisation events may have catastrophic effects, if seen from the perspective of species extinctions caused by them. This was the case in the Great American Interchange, which took place about three million years ago, when the bridging of the Isthmus of Panama allowed placental mammals to move south and marsupials north (Webb 1991). But, given enough time, diversity increases once again. Within the context of alien invasives, we are obliging species that have never encountered each other to share ecological space, and yet we wish to maintain the diversity of forms that were present before the introductions. And this is within ecological, not evolutionary, time. Ultimately, the question really boils down to what we want our ecosystems to look like, and which species we wish to share our space with. There is no correct ecological or evolutionary answer to this. At best, ecology (the study of species interactions in the here and now) and evolution (the study of genetic consequences of these interactions across multiple generations) may help us to predict what sorts of influence alien invasive plants and animals could have on our landscape. *** In this chapter, we have examined the long history of mammals in Africa, which goes back some 200 million years and is more remarkable than often depicted. 77

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Mammals evolved from a reptilian-like therapsid ancestor but remained small and somewhat undifferentiated until the demise of the dinosaurs 66 million years ago. In the long period leading up to this critical event, however, mammals did occasionally undergo modest levels of diversification, as evident from studies of the multituberculates. We have also looked at how the mammalian fauna of Africa has changed over time, with the arrival of new forms through colonisation and the loss of others through extinction. However, the composition of African mammals is not simply dependent on colonisation events but also involves local radiations and speciation. The next two chapters deal with this topic, by looking first at the special case of islands (chapter 4) and then at the situation on mainland Africa (chapter 5).

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CHAPTER

4

Islands as Species Factories

W

e often view islands as beautiful retreats where a city-weary humanity can forget about the pressures of day-to-day life. However, islands are also valuable destinations for ecologists and evolutionists. Historically, indeed, they have been pivotal to our understanding of evolution: it was the natural history of the Galápagos Islands, after all, that inspired Charles Darwin’s theory of evolution by natural selection – and Darwin himself was heavily influenced by the work of Alfred Russel Wallace, who had already arrived at similar conclusions in the Malay Archipelago. The advantage of islands for the evolutionist is that their ecosystems are relatively simple, so otherwise complex ecological interactions are much easier to study than in their mainland equivalents. This makes perfect sense when one recognises that for any terrestrial organism to inhabit an oceanic island, its ancestors must have travelled across open water to get there.1 Such a challenge immediately limits the number and kinds of organisms that are likely to make and survive the journey. Birds and bats are both well represented on islands, their powers of flight enabling them easily to cross over from the nearest mainland. Frogs, typically, are not: not only do they lack wings, but also their permeable skin does not tolerate immersion in salt water for even short periods. By this measure, rodents and terrestrial reptiles are intermediate in their ability to colonise islands – doing so by rafting across the sea on floating debris (as discussed in chapter 3). Although such a journey may appear implausible – and

79

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in fact, it is implausible! – we need to remember that 100 000 years in evolutionary terms is the mere blink of an eyelid. Over such prodigious amounts of time, even the most improbable event is likely to happen – even if only once. In the words of celebrated US palaeontologist George Gaylord Simpson, ‘any event that is not absolutely impossible … becomes probable if enough time elapses’ (cited in Krause 2010: 613–614). Islands have two fundamental features that ultimately determine the number of species that inhabit them: their size and their distance from the mainland. Larger islands are more likely to be accidentally colonised, because the chances of running ashore on a larger landmass are greater than those of doing so on a smaller one. Similarly, an island close to the mainland is more likely than one further away to receive colonists, because the chances of surviving a short journey across open ocean are higher than those associated with a protracted one. By introducing one more factor, extinction, we can turn our theory into a predictive model of how many species we should expect on an island. We expect a large island to retain greater numbers of a species than a smaller one, because species tend to become extinct more quickly on smaller islands, by virtue of their smaller populations. By combining the probabilities of colonisation and extinction, Edward Wilson and Robert MacArthur in 1967 first propounded the celebrated ‘theory of island biogeography’ (Wilson and MacArthur 1967). This beautiful theory – beautiful because of its economy – has been extensively tested and nearly always holds. When it does not hold, this has been because of some disturbance – anthropogenic or otherwise – that has ‘reset’ the number of species to a lower value than predicted.

AFRICAN ISLANDS The best-known African island must be Madagascar, both because of its great size and because of the many bizarre creatures that inhabit its forests. Madagascar is so large, in fact, that some have argued for its status as a continent. Traditionally, it ranks as the fourth-largest island in the world (following Greenland, New Guinea and Borneo), stretching some 1 100 kilometres from north to south and almost 500 kilometres from east to west. Madagascar, you will recall from chapter 3, was once part of the southern landmass known as Gondwana but has been totally isolated for 90 million years and separated from 80

Islands as Species Factories

mainland Africa for more than 150 million years. This isolation has played a decisive role in the evolution of its mammals, as we shall see later in this chapter. Therefore, although Madagascar may be of continental origin, it is – as far as mammalian evolution is concerned – effectively oceanic. This is because all the mammals that currently reside there evolved after it had split away from Gondwana. Hence, all native Malagasy mammals are descendants of African ‘colonists’ that found their way across the Mozambique Channel, which is over 400 kilometres wide at its narrowest point. Between Madagascar and Mozambique, the nearest point on the African mainland, lie the Comoros, a chain of four volcanic islands that somewhat bridges the gap – although Mayotte, the closest island, is still more than 300 kilometres from Madagascar, which constitutes a considerable sea journey for any terrestrial mammal. From west to east, the islands are Grande Comore, Mohéli, Anjouan and Mayotte (figure 4.1).2 This sequence also represents their incremental ages: Grande Comore is the youngest, at no more than half a million years old, while Mayotte, which formed 15–10 million years ago, is the oldest. East of Madagascar lies the Mascarene archipelago, comprising La Réunion,

Kenya

Pemba Unguja

Mahé (Seychelles)

Mafia

Tanzania

Aldabra Anjouan Mayotte

Indian Ocean

Grande Comore Mohéli ue

biq

am

Madagascar

oz

M

Mauritius

Mozambique Channel

Rodrigues

La Réunion

0

250

500km

Figure 4.1. Map of the western Indian Ocean islands mentioned in this chapter.

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Mauritius and Rodrigues, all of which are volcanic in origin and between two and seven million years of age. North of Madagascar are the 115 islands that make up the Seychelles. Almost half of these islands are granitic in nature and constitute the ‘debris’ left in the wake of India’s race north after splitting from Madagascar during the break-up of Gondwana. Three other islands worth mentioning, also off Africa’s east coast, are Unguja, Pemba and Mafia, although none of them is associated with the Seychelles.3 There are also many coral atolls in this region of the ocean – ‘extinct’ islands that have submerged slowly over eons, allowing their fringing coral reefs to continue building up. These corals, which are living structures, cannot survive at great depths, so if an island sinks too rapidly the corals die with it. Off the west coast of equatorial Africa, the Gulf of Guinea harbours several islands, all volcanic in origin. The four largest are Bioko, Principe, São Tomé and Annobón.4 These form part of the Cameroon Volcanic Line, which runs for some 1 600 kilometres, hugging the border between Cameroon and Nigeria before disappearing into the sea to the south-west; Mount Cameroon, which is 80 kilometres from Bioko, is part of this volcanic system. We will return to the Cameroon Volcanic Line in chapter 5. There are many other islands associated with Africa, including Socotra, in the Arabian Sea; the Canary Islands, in the North Atlantic Ocean; and Tristan da Cunha and Prince Edward islands in the South Atlantic Ocean and subAntarctic Indian Ocean, respectively. However, these islands all either have no native mammals (the South Atlantic and sub-Antarctic Indian Ocean islands), or their mammals colonised them from Europe and therefore share a history with that continent rather than with Africa.

AFRICA’S ISLAND MAMMALS So what do Africa’s islands have to tell us about the story of Africa’s mammals? The more remote islands, such as those in the South Atlantic and sub-Antarctic Indian Oceans mentioned above, do not have native terrestrial mammals of any kind.5 The closest of these islands is more than 2 200 kilometres away from Africa, surrounded by chilly waters and situated in the Roaring Forties (a belt of typically strong westerly winds circumscribing the globe at 40–50 degrees latitude, south of the equator). We should therefore not be surprised that even bats 82

Islands as Species Factories

failed to make it here! The Mascarene and Seychelles islands have a few species of bat, but no terrestrial mammals, which is also the case with Socotra. The Canary Islands are home to a single native terrestrial mammal, an insectivorous shrew (Crocidura canariensis) that traces its ancestry to Europe, plus, unsurprisingly, a couple of bat species.6 In contrast, the Gulf of Guinea islands off the west coast, and Zanzibar and Mafia off the east coast, have well-established though greatly depauperate mammalian faunas. Madagascar, because of its great size (300 times larger than Mauritius), bears little comparison with these other islands, and we will deal with it separately later in this chapter. Islands off Africa’s east coast So far so good – we have established a broad relationship between the remoteness of an island and its mammalian fauna. But does this relationship hold up to more detailed scrutiny? One way of conducting such an analysis would be to determine whether the number of species on an island is influenced by its size and/or distance from the mainland. We could start by listing the islands in order of distance from the mainland. The Mascarene Islands are the most remote archipelago, with Rodrigues being furthest out, followed by Mauritius and then La Réunion. None of these islands has ever had any terrestrial mammals that were not introduced by humans, but all three support native bats. Rodrigues has one species, Mauritius three and La Réunion four (O’Brien 2011), just as theory would suggest. Next, let’s consider the granitic island of Mahé and the atoll Aldabra, which both belong to the Seychelles. Mahé is approximately 1 750 kilometres off the coast of Africa whereas Aldabra is just 630 kilometres away, and their respective numbers of bat species are two and four; as expected, the more remote Mahé has fewer species. But Mahé, about the same distance away from the mainland as La Réunion, supports only half as many bat species as La Réunion. This would seem at first to spoil the rather neat relationship between species richness and distance of an island from the mainland. But if we now consider the sizes of the islands, we will notice that La Réunion is more than ten times larger than Mahé – which means the relationship still holds. Table 4.1 gives details of the islands associated with Africa and their bat assemblages. To complete the picture off the east coast, let’s examine the mammalian fauna of the three islands just off Tanzania: Mafia, Unguja and Pemba, which are about 20, 40 and 60 kilometres offshore respectively. All three islands have a diverse 83

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Table 4.1. Islands associated with Africa, their size and distance from the ­mainland, and number and composition of the bat fauna.

Island

Distance Number from African of bat Size (km2) mainland (km) species

Bat species and key references

Mascarenes (Rodrigues)

108

2 600

1

Pteropus rodricensis (O’Brien 2011)

Mascarenes (Mauritius)

2 040

2 000

3

Pteropus niger, Mormopterus acetabulosus, Taphozous mauritianus (O’Brien 2011)

Mascarenes (La Réunion)

2 500

1 800

4

Pteropus niger, Mormopterus francoismoutoui, Taphozous mauritianus, Scotophilus borbonicus (O’Brien 2011)

Seychelles (Mahé)

175

1 750

2

Pteropus seychellensis, Coleura seychellensis (O’Brien 2011)

Seychelles (Aldabra)

155

630

4

Pteropus aldabrensis, Triaenops pauliani, Taphozous mauritianus, Chaerephon pusillus (O’Brien 2011)

Comoros (Mayotte)

368

450

4

Pteropus seychellensis, Taphozous mauritianus, Chaerephon leucogaster, C. pusillus (Goodman et al. 2010)

Comoros (Anjouan)

424

380

8

Pteropus livingstonii, P. seychellensis, Rousettus obliviosus, Chaerephon pusillus, C. leucostigma, Myotis anjouanensis, Miniopterus griveaudi, M. aelleni (Goodman et al. 2010)

Comoros (Mohéli)

211

330

5

Pteropus livingstonii, P. seychellensis, Rousettus obliviosus, Chaerephon pusillus, C. leucostigma (Goodman et al. 2010)

Comoros (Grande Comore)

1 025

300

4

Pteropus seychellensis, Rousettus obliviosus, Chaerephon pusillus, Miniopterus griveaudi (Goodman et al. 2010)

Zanzibar (Unguja)

1 650

40

22

Plus 23 terrestrial native mammals (Pakenham 1984)

Zanzibar (Pemba)

990

60

17

Plus 8 terrestrial native mammals (Pakenham 1984)

(Continued ) 84

Islands as Species Factories

Island Mafia

Distance Number from African of bat Size (km2) mainland (km) species

Bat species and key references

400

20

14

Plus 25 terrestrial native mammals (Goodman et al. 2010; Kock and Stanley 2009)

2 017

32

26

Plus 39 terrestrial mammals (Jones 1994; Juste and Ibanez 1994)

Gulf of Guinea (Principe)

136

220

4

Plus Crocidura poensis (Jones 1994; Juste and Ibanez 1994)

Gulf of Guinea (São Tomé)

854

280

9

Plus Crocidura thomensis (Jones 1994; Juste and Ibanez 1994)

Gulf of Guinea (Annobón)

17

340

2

Myonycteris brachycephala, Chaerephon thomensis (Jones 1994; Juste and Ibanez 1994)

Gulf of Guinea (Bioko)

bat community comprising a dozen or more species. In addition, each is home to between 8 and 25 terrestrial species of mammal (Kock and Stanley 2009; Pakenham 1984). As expected, the highest diversity of terrestrial mammals is on the island closest to the African mainland (Mafia) and the lowest is on Pemba, which is the furthest away. Now, let’s introduce the Comoros. Remember that this archipelago comprises four islands, and their bat assemblages from west to east (that is, at increasing distances from the African mainland) consist of four, five, eight and five species, respectively (Goodman et al. 2010). The neat relationship we established seems to have broken down; the closest island does not have the greatest diversity. What is going on here? There are two key details that might help to explain things. The first is that the four islands are, from a bat perspective, geographically close together, with neighbouring islands separated by distances of just 40 to 80 kilometres. This distance is short enough that the bat species that occur on multiple islands have not differentiated ­genetically from each other.7 They are able – on occasion, and presumably by a­ ccident – to travel between the islands, thus ensuring that there is sufficient genetic mixing for no one species to be distinguishable from another. The second 85

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detail is that the bats have colonised the Comoros not from Africa but from Madagascar! Of the ten bat species occurring in the Comoros, five are shared with Madagascar, and another three have their closest relatives on Madagascar. The remaining two species are Pteropus species – the large fruit-eating bats, known as flying foxes, which originated in Asia. Hence, it would appear that not a single one of the bat species on the Comoros was seeded from mainland Africa. Thus we assume that African bats must first have colonised Madagascar and, from there, moved on to the Comoros and then the mainland. An alternative explanation – but a less likely one, as it depends upon more untested assumptions – is that these bats reached the Comoros from Africa, where they differentiated into new species that then went on to colonise Madagascar. A further important observation regarding the Comoros is that Mayotte, which is the closest of the four islands to Madagascar, is also the oldest. As a result, its landscape is more heavily eroded and thus devoid of natural caves, a critically important roost for several of the bat species of this archipelago. Hence, the island with the highest diversity of bats is Anjouan, the one secondclosest to Madagascar. Once we understand the underlying complexities, things begin to make sense again. Islands off the west coast of mainland Africa What about the islands off Africa’s west coast – those in the Gulf of Guinea (figure 4.2)? I have not included them in our discussion of the east coast island groups, because their source population of bats and/or terrestrial mammals is rather different. The bats off Africa’s east coast are mostly species associated with savanna habitats, whereas those off the west coast are tropical forest species. If we conduct a similar (and equally rough) analysis for the Gulf of Guinea islands, we will find a similar trend, with an interesting twist. The four main islands are, respectively, 32, 220, 280 and 340 kilometres offshore. Bioko, the closest, has 65 species of mammal in total, of which 26 are bats. Principe has four bat species and one native shrew (Crocidura poensis), which is fewer than the nine bat species and one shrew species (Crocidura thomensis) that inhabit the more distant, but six times larger, São Tomé. Annobón, the most remote, has no terrestrial mammals and just two species of bat (Jones 1994; Juste and Ibanez 1994). So, the patterns are much the same as we saw off the east coast 86

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Nigeria Mount Cameroon Bioko

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Figure 4.2. Map of the islands of the Gulf of Guinea and Mount Cameroon.

of Africa, except that Bioko is noticeably richer in species, especially terrestrial mammal species. Why should this be? It is farther offshore than Mafia (off the east coast) but has almost twice the mammalian diversity. The reason is that Bioko was connected to Africa during the Last Glacial Maximum (LGM) and therefore would then have received a full complement of the mammals occurring in that part of the continent.8 But a direct comparison of Bioko with a similar patch of mainland forest – say, in Equatorial Guinea – is telling, because Bioko has many fewer species. Interestingly, we see the same pattern on the east coast in the two Zanzibari islands and Mafia. Of these three islands, Unguja and Mafia were connected to the mainland during the LGM, but Pemba has been isolated for millions of years (Prendergast et al. 2016). As a result, there are only 8 species of terrestrial mammals on Pemba, compared with 23 and 25 on Mafia and Unguja, respectively. From this rather superficial examination, we can conclude that the mammal fauna on Africa’s islands offers abundant evidence to support the theory of island biogeography. We have not included in our analysis the age of the islands or catastrophic disturbances (such as volcanic eruptions) that would 87

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have impacted on the nature of the relationship we have just investigated. Nor have we taken into account the recent extinctions that have beset some of these islands. For example, the lesser Mascarene flying fox (Pteropus subniger) was hunted to extinction on both Mauritius and La Réunion by humans in the 1860s or 1870s.9 Further, I have implicitly assumed that all colonists to these islands arrived from Africa, but this is not always the case. For example, the flying foxes of the genus Pteropus are not African in origin. This genus is widely distributed in Australasia and tropical Asia, whence they colonised the western Indian Ocean Islands (O’Brien et al. 2009). By examining the genetic relationships between these various Pteropus species, John O’Brien and his colleagues suggest that three separate waves of immigration took place. The first wave, from the Indian subcontinent, carried this genus to Pemba Island and the Comoros Islands; the second wave, probably from South East Asia, seeded the Mascarene Islands of Rodrigues; and the final wave, again from India, seeded the remaining islands, including the Comoros (for a second time), the Seychelles, Madagascar, La Réunion and Mauritius. Another genus that clearly colonised from the east is the insectivorous free-tailed bat of the genus Mormopterus. On balance, though, most of the mammalian colonists on these islands, including bats, arrived from Africa.

MADAGASCAR: EVOLUTION IN MICROCOSM I would now like to turn our attention to another major factor that influences species diversity on islands: in situ speciation. I have talked about bats on islands as if they were all the same species as those on the mainland of Africa. Although this is true for some species, such as the Egyptian tomb bat (Taphozous mauritianus), which occurs in Mauritius, Madagascar and throughout Africa, others are endemic to single islands or island groups. This is because these bats, upon colonising an island, proceeded down a quite separate evolutionary path from that of their mainland cousins. Over time, these island populations have diverged sufficiently to be considered specifically distinct (see chapter 2 for a discussion of the workings of speciation). This process is not restricted to bats but influences speciation in numerous groups of island mammals. It is most beautifully illustrated in Madagascar, where just four colonisation events seeded all 168 species of native terrestrial mammal that now occur on the island 88

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(Poux et al. 2005). These four groups are the rodents, tenrecs, carnivores and primates, and each group represents an impressive example of adaptive radiation – the process whereby a single founding species diversifies rapidly into multiple new species to fill available niches. (We will deal with the concept of a niche in more detail in chapter 7.) Bats are a diverse and interesting component of Madagascar’s mammalian fauna, but their history is complicated by multiple colonisation events. We will return to them later in this chapter. It has been possible to date the four colonisation events of Madagascar’s terrestrial mammals by comparing the DNA of modern representatives of each of the four groups with their closest relatives on mainland Africa. The sequence of arrivals is as follows: primates (represented by lemurs in the endemic family Lemuridae), 60–50 million years ago; tenrecs (represented by three endemic subfamilies in the Tenrecidae), 42–25 million years ago; carnivores (represented by the endemic Eupleridae, figure 4.3), 26–19 million years ago; and finally rodents (represented by the endemic subfamily Nesomyinae), 24–20 million years ago. You will notice that there is a large range in the putative dates of arrival, and this reflects the uncertainties of such molecular analyses. But this

Figure 4.3. A fossa (Cryptoprocta ferox), an example of a euplerid carnivore, the whole family being endemic to Madagascar. Photograph by Ara Monadjem.

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uncertainty refers only to the exact date of arrival, not to the process of arrival itself. What is certain is that each of these groups is a clade, meaning that for any of them, all the current species in Madagascar are descended from a single ancestor. Hence, all the lemurs (the only primates in Madagascar) have radiated from one immigrant individual (for example, a pregnant female), or a small group of individuals, that arrived on the island between 60 and 50 million years ago. Similar stories recount the history of Madagascar’s rodents, tenrecs and carnivores. Rapid species radiation on Madagascar What makes Madagascar different from other western Indian Ocean islands is that its original colonisation event was followed by rapid species radiation. This is not evident on any of the other western Indian Ocean islands, all of which are very much smaller. Take the rodents. All native Malagasy species belong to the family Nesomyidae, which is widely distributed across mainland Africa and has its greatest diversity in southern Africa. This diverse family comprises six subfamilies, with five occurring on the mainland and the sixth (the Nesomyinae) endemic to Madagascar. The mainland species range from the giant rats of the genus Cricetomys, which grow to the size of a small cat, to the climbing mice of the genus Dendromus, which top the scale at around 6–10 grams and are no larger than your thumb, if you discount the long, prehensile tail. Sometime around 22 million years ago, perhaps a single pregnant female nesomyid – or, at most, a small group of individuals – rafted across the Mozambique Channel on favourable currents.10 Thus began the occupation of the island by rodents. Today, there are 27 species of nesomyid rodent in Madagascar, all the descendants of that single colonisation event. So why did Madagascar produce such a spectacular radiation when other African islands did not? The reasons are probably twofold. First, Madagascar is vastly larger than any other African island and, thanks to its great variety in climate and topography, from semi-arid spiny desert in the south-west to mountainous rainforest in the north-east, it offers a wide range of habitats and hence ecological niches for potential occupation. Second, Madagascar is older than most other African islands, and this has provided the requisite time frame in which evolutionary processes can unfold. Remember that Madagascar has been completely isolated for 90 million years (and separated from Africa for more 90

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than 150 million years), whereas, for example, the Comoros, Gulf of Guinea and Mascarene Islands are all less than 15 million years old – and most of them far younger, particularly if you consider recent volcanic activity that would have made many of them uninhabitable until the past few hundred thousand years. Madagascar’s 27 extant rodent species belong to 9 distinct genera and exhibit a large variety of body forms. The largest is the giant jumping rat (Hypogeomys antimena, figure 4.4), which is the size of a large rabbit, has a short tail, is entirely terrestrial and digs its own burrows. At the other extreme, naked-tailed forest mice of the genus Voalavo weigh just 20 grams and have a long, thin tail that they use when climbing forest plants and lianas. Among the many other forms in between are some that resemble squirrels (Nesomys), gerbils (Macrotarsomys) and even northern-hemisphere voles (Brachyuromys) (Goodman and Monadjem 2017). Indeed, the variety of forms displayed by Malagasy rodents confused early systematists into believing that they must be the evolutionary result of multiple colonisations of the island. Thanks to recent molecular techniques, we now know that they form a single clade and that the similarity with other rodents is due to convergent evolution. This is

Figure 4.4. A giant jumping rat (Hypogeomys antimena) at Kirindy Mitea National Park, western Madagascar. Photograph by Ara Monadjem.

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the process whereby species from separate and often very different evolutionary lineages develop similar physical characteristics as a result of adapting to shared or similar environmental challenges. For example, the armadillos of the New World are completely unrelated to the pangolins of the Old World. The two evolved separately on different parts of the planet and are today classified within separate orders (Cingulata and Pholidota, respectively). However, both have adapted, separately, to the challenge of subsisting on ants and termites, and as a result have acquired a number of similar physical traits – including an armoured body that they can roll into a ball for defence, powerful spade-like front claws for excavating ant hills and a long sticky tongue for harvesting their prey. It is understandable, then, that the layperson might think them related – and indeed, in popular culture they are often confused. In some ways, the tenrecs present even more startling examples of convergent evolution. Tenrecs (family Tenrecidae), if you recall, are members of the Afrotheria (see chapter 3). The family is entirely restricted to Madagascar, its closest relatives being three species of otter-shrew (family Potamogalidae) restricted to the tropical forest zone on mainland Africa. The Malagasy tenrecs are allocated to three subfamilies, all endemic to the island: the Tenrecinae, Oryzorictinae and Geogalinae. Some members of the tenrecines are covered with spines and resemble hedgehogs, while the common tenrec (Tenrec ecaudatus) could be confused with an opossum – a marsupial! The oryzorictines resemble shrews, and the large-eared tenrec (Geogale auritus), the only living member of the subfamily Geogalinae, appears to have been assembled from body parts randomly borrowed from mice and shrews. The African otter-shrews are a bizarre collection of three semi-aquatic species. The giant otter-shrew (Potamogale velox) is a relatively large animal, reaching 60 centimetres in length, that – as the name suggests – vaguely resembles a cross between an otter and a shrew. It uses its laterally flattened tail to propel itself through water in pursuit of fish, frogs and crustaceans in the tropical rivers and streams of central African rainforests. The two smaller species of the genus Micropotamogale are rat-sized and have highly restricted distributional ranges, with one in the Albertine Rift (east Africa) and the other at Mount Nimba (west Africa). Both forage in streams for crabs, and although neither has a flattened tail, the Albertine Rift species has webbed feet, which suggests an adaptation to aquatic life. Interestingly, the two Micropotamogale species were discovered only in the mid-1950s, which reflects the elusive nature of their lifestyles (Monadjem 2018). 92

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If we examine the distribution of extant species of the tenrec family, we could be excused for thinking that this is an exclusively Malagasy group, from which the three otter-shrews evolved and subsequently colonised the African continent from Madagascar. However, the molecular evidence tells a different story. The African Potamogalidae are basal to the phylogenetic tree of the tenrecs; in other words, they represent the ancestral form. This tells us that the ancestors of tenrecs (which were also the ancestors of the extant Potamogalidae) were once widely distributed in Africa, but – except for the three species of ottershrew – have now become extinct. The reasons are not clearly understood, but it is a curious fact that all three African ‘tenrecs’ (the otter-shrews) are aquatic. Perhaps these were the only ones that could hold their ground against the colonisation by true shrews, unrelated to tenrecs, which – along with many other mammals – colonised Africa from Eurasia (see chapter 3). Species diversity: The lemurs of Madagascar For the most impressive example of species diversity among Madagascar’s mammals, you need look no further than its most iconic residents: the lemurs. Today, at least 105 species inhabit the island, ranging from the muchcaricatured ring-tailed lemur (Lemur catta) – think of King Julien XIII in the movie Madagascar – to the hooting, tail-less indri (Indri indri, figure 4.5a), the diminutive mouse-lemurs of the genus Microcebus and the bizarre-looking aye-aye (Daubentonia madagascariensis), which digs out insect larvae from branches using the specially attenuated third digit of its hand. These exceptionally diverse primates occur nowhere else on Earth and occupy virtually every terrestrial habitat on the island. Some are nocturnal (Lepilemur) and some diurnal (Eulemur); some are mouse-sized (Microcebus), some cat-sized (Propithecus, figure 4.5b) and some recently extinct species (Archaeoindris) weighed as much as a gorilla; some have diets that include vertebrates (Mirza), some specialise in tree gum (Phaner) and some are strict vegetarians (Indri). Amazingly, however, all are descended from a single common ancestor (Herrera and Davalos 2016), which colonised Madagascar just once. Since this ancestral lemur evolved on the African mainland at least 30 million years after the isolation of Madagascar, it must have crossed several hundred kilometres of the Mozambique Channel to reach the island. This journey seems implausible today, given that the ocean currents presently move down the coast of Africa and from east to west across 93

(a)

(b) Figure 4.5. Lemurs: (a) An indri (Indri indri ) at Andasibe-Mantadia National Park and (b) a Verreaux’s sifaka (Propithecus verreauxii ) at Kirindy Mitea National Park. Photographs by Ara Monadjem.

Islands as Species Factories

the Mozambique Channel (Stankiewicz et al. 2006). In other words, rafting today might be possible from Madagascar to Africa but not vice versa. However, it appears that during the Palaeocene, when the ancestral lemur made its epic journey (Ali and Huber 2010), these currents flowed in the opposite direction. Considering the configuration of present-day ocean currents, it is rather surprising that lemurs – or any of the other native Malagasy mammals – have not made the reverse journey to their ancestral homeland. Perhaps some did, but could not survive the competition they encountered when they arrived there? So what happened to lemurs on mainland Africa? Today, the niches they once occupied have been taken over by monkeys and apes. It was the evolution and rapid radiation of these more advanced primates that brought about the demise of lemurs, which found themselves unable to compete – just as clovenhoofed antelopes once outcompeted the hyracoids (see chapter 3). In effect, therefore, the lemur diversity in Madagascar offers a window onto one stage of mainland Africa’s distant primate past. Today, the closest relatives of lemurs on the mainland are members of the superfamily Lorisoidea (galagos, pottos and angwantibos). These diminutive primates have managed to avoid competition with monkeys by adopting more secretive, nocturnal lifestyles. Bat colonisations of Madagascar The last Malagasy group that I will consider here has a rather different history from those of the terrestrial mammals described above. This is the bats. As we have seen throughout this chapter, bats are good colonisers because their power of flight enables them to cross open oceans. Therefore, in contrast to the four earth-bound mammal groups, bats have colonised Madagascar on numerous occasions. As a result, their story is more complex and involves both multiple colonisation events and several adaptive radiations. The most impressive example of the latter must surely be that of the genus Miniopterus (family Miniopteridae). In 1995, just 4 species were known on the island. Since then, 8 additional species have been described by the tireless Steve Goodman (figure 4.6) and his collaborators (Goodman, Ramasindrazana et al. 2015), raising the total to 12, with rumours of one or two more taxa that may still be overlooked. Whether this radiation represents colonisation by a single ancestral Miniopterus from Africa, or whether there were multiple colonisation events is, unfortunately, not known. The molecular 95

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Figure 4.6. Steve Goodman (second left) regaling students on a Tropical Biology Association field course at Kirindy Mitea National Park, western Madagascar, in 2014. Photograph by Ara Monadjem.

analyses conducted thus far have not resolved this mystery (Schoeman et al. 2015). What is known, however, is that two of these species (Miniopterus grivaudi and M. aelleni) also occur on the Comoros, hence there must be regular dispersal across the 300-kilometre channel between the islands. In contrast, none of the 12 Malagasy species has a close relative on mainland Africa. A slightly different pattern is shown by another bat family in Madagascar, the pipistrelloid group of the family Vespertilionidae. In this group – ­effectively the LBJs, or ‘little brown jobs’, of the bat world (to use birding parlance), because they are so difficult to distinguish – some six species are known from the island. One of these (Pipistrellus hesperidus) is shared with mainland Africa; the rest are Malagasy endemics. However – and here is the interesting point – the closest relatives of most of these Malagasy endemics are species that occur on mainland Africa, which strongly suggests multiple 96

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colonisations of Madagascar by these bats. A similar pattern can be seen in the free-tailed bats of the family Molossidae. These are typically longwinged, fast-flying bats, capable of long-distance travel. Despite the fact that the smaller species weigh just 10 grams, tracking studies have shown that they can easily travel 10 to 20 kilometres in a straight line in a couple of hours (Noer et al. 2012), making them ideal candidates for long-distance dispersal. One of the larger molossid species, the Midas free-tailed bat (Mops midas, figure 4.7), is a large insectivorous species with a wingspan of half a metre that demonstrates practically no genetic differentiation between populations in southern Africa and Madagascar, which strongly suggests that there has

Figure 4.7. A Midas free-tailed bat (Mops midas), a large molossid bat that occurs both in Madagascar and mainland Africa with little genetic differentiation between these populations. The animal was roosting in the roof of a house. Photograph by Ara Monadjem.

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been regular mixing between the two (Ratrimomanarivo et al. 2007; Samonds et al. 2012). This can only have come about through bats moving from mainland Africa to Madagascar, and/or vice versa, and over an ecological rather than geological timescale – say, over tens or hundreds of years, rather than thousands. Other molossids, however, appear to have colonised Madagascar just once, as is probably the case with Mops leucostigma. The closest relative of this Malagasy and Comoros endemic is the Angolan free-tailed bat (Mops condylurus), which occurs widely across sub-Saharan Africa. The ancestral M. leucostigma individual, or small group, must have made it across the Mozambique Channel, perhaps using the Comoros as a stepping stone. However, since this Malagasy species is clearly distinguishable from the mainland species, there could not have been any further genetic exchange between them. Thus, as in the family Vespertilionidae, but possibly unlike the case of the Miniopteridae, there have been multiple colonisation and radiation events in the family Molossidae. *** In this chapter we have examined the different ways in which mammals have been able to colonise Africa’s offshore islands. The simplified ecosystems of these islands allow us to study in detail evolutionary processes that are often too complex to tease out on the mainland. Bats, because of their ability to fly, have been able to colonise islands more effectively than terrestrial groups such as rodents or carnivores – although these earth-bound mammals are able, over significant periods of time, to colonise islands by rafting across the sea on floating debris. The location of an island has a bearing on the colonisation process, with more remote islands being more difficult to colonise than those closer to the mainland. The size of an island is also a factor, with larger islands offering greater habitat and climatic variety, and thus more ecological opportunities for new species to evolve. Other factors also play a role, including the age of the island, its past connectivity to the mainland and its proximity to other islands. In the next chapter we will examine some of these same evolutionary processes as they have taken place on Africa’s mainland.

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5

Evolution on the African Mainland

I

n the previous chapter, we saw that islands allow us a simplified view of how localised movements between animal populations can promote genetic divergence. Being discrete entities – for terrestrial mammals, at least – they are perfect for studying the rather complicated process of evolution. An animal either makes it to an island or perishes along the way. It is an ‘all or nothing’ situation; there is no halfway house. This is not the case on the mainland. Here, an animal may move from one geographic location to another, or it may move half that distance, or a third or a fifth. As long as there is suitable habitat and a corridor to travel along, it can hypothetically move any distance between the maximum of which it is capable – which will largely be determined by its inherited features, such as its size and means of locomotion – and no distance at all. Thus, on the mainland, trying to untangle the various colonisation events and distinguish them from local radiations is a much messier affair than on islands. But we can still piece together the story of how mammals on the African continent ended up where we find them today, and you will see that it is, in its own way, just as fascinating as the stories that unfolded on its associated islands. MOVEMENTS AND BARRIERS No animal species is spread across the entire planet – although a few species, including our own, have done their best to achieve that. Each occurs in 99

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a particular defined region, which is known as its ‘distribution’ or ‘range’. The patterns of these distributions are determined by a variety of factors. On a local scale – say, within a large national park – species tend to be segregated by habitat (we will look more closely at this in chapters 6 and 7). However, on a global or continental scale there is often little relationship between habitats and species – as is clear from the glaring absence of species on one continent that appear in very similar habitat on another. Why, for example, are there no tigers or tapirs in the Congo Basin? Attempting to identify and explain distributional patterns on a broader scale is the task of biogeography, which helps us understand the history of a species – or an ecosystem – through geological time and geographic space, and incorporate this into its ecology. In this way, we can make sense of apparent anomalies. For example, the magnificent sable antelope (Hippotragus niger) graces the savannas of southern and east Africa but is curiously absent from similar habitat in west Africa, while its close relative the roan antelope (Hippotragus equinus) occurs throughout this region, including in west Africa (figures 5.1a–c), and a third close relative, the extinct blue antelope (Hippotragus leucophaeus), occurred only in a small area at the extreme southern tip of South Africa (Kerley et al. 2009).1 Why should three such similar species exhibit such radically different distribution patterns? To address this question, we must first apply some of the principles we learned from studying island populations (see chapter 4). In particular, we need to consider how mammals have dispersed across the continent, crossing imposing topographical barriers – the equivalent of the ocean for those island colonists – in order to colonise new ‘islands’ of habitat. A good starting point is to identify what barriers mainland mammals might encounter. Generally speaking – and with the possible exception of bats – four things can restrict the movement of most mammals: mountains, rivers, vegetation (or the lack of it) and climate. The barriers presented by high mountains and wide, fast-flowing rivers are self-evident. For a species adapted to lowland habitats, a high mountain is a major impediment and a mountain range may effectively block its progress in a particular direction. Similarly, though most mammals are adept swimmers, large rivers are formidable obstacles. The Congo River, for example, is 5 to 10 kilometres wide along several thousand kilometres of its length, with very strong currents that all but rule out the possibility of a mammal making it across. The barriers presented by vegetation and climate may be less immediately visible, but are just as substantial. For an arboreal forest 100

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Figures 5.1. (a) Distributions of roan (Hippotragus equinus) and sable (H. niger) antelopes based on information from the IUCN (2019). Grey shading indicates the distribution of roan and grey stippling the distribution of sable. A roan antelope (b) and sable antelope (c), both in Hwange National Park, Zimbabwe. Photographs by Mike Unwin.

species such as the forest giant squirrel (Protoxerus stangeri), for example, which forages singly in the forest canopy in search of fruit, even a short stretch of open savanna represents a hostile environment where the risk – or fear – of predation 101

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is greatly magnified. Correspondingly, for a typical savanna species, a forest patch might as well be an ocean. Climate, meanwhile, may present conditions, such as extremes of heat or cold, that a mammal’s physiology has not evolved to deal with. Since vegetation interacts in a complex way with climate, soils, herbivory and fire (see chapter 6), its distribution across the landscape is continuously changing. To complicate the picture, mountains, rivers, vegetation and climate are inextricably linked with each other. It is thus often not easy to tease out the root cause of a barrier. In the case of a mountain, is it a barrier because of its steep slopes, the cold nights at the top, the open grasslands on the plateau or, perhaps, some combination of the three? Whatever the answer, it makes the mountain no less of a barrier! What then are the main barriers to mammal dispersal within an African context? The celebrated zoologist and author Jonathan Kingdon has suggested that Africa’s dominant biogeographic feature is the tropical rainforest belt that runs east to west, from Uganda to Sierra Leone, and divides the moist savannas that are aligned roughly north to south, from Ethiopia to South Africa (Kingdon et al. 2013). Undoubtedly, this is an important consideration, as many species of mammal show distributions that are limited by this boundary, despite there being suitable habitat on the other side of it. For example, many species of bat, rodent, shrew, primate, carnivore and antelope occur throughout the forest block of central and west Africa, but fail to make it across to forests of the Eastern Arc Mountains of Tanzania, presumably because they have failed to disperse across the extensive savannas and grasslands of east Africa. Furthermore, many species that occur throughout the forest belt are replaced by closely related sister species in the savanna block. Such ‘species pairs’ include the savanna and forest elephants (Loxodonta africana and L. cyclotis), the bushpig and red river hog (Potamochoerus larvatus and P. porcus), the southern and western tree hyraxes (Dendrohyrax arboreus and D. dorsalis), and the red-legged and mutable sun squirrels (Heliosciurus rufobrachium and H. mutabilis), to name just four. In fact, there are dozens of such examples among mammals, and also plenty among birds and reptiles. The Albertine Rift transition zone The exact location of this forest-savanna boundary is a matter of some debate, but the Albertine Rift appears to be where many of the transitions between 102

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forest and savanna forms take place. Since this zone is recognised as a key biodiversity ‘hotspot’ (we will return to hotspots later in this chapter), and is not particularly well known – even amongst biologists – it is worth giving it some attention here. The Albertine Rift forms part of the Great Rift Valley, effectively a long continuous crack in the earth’s crust that extends between Israel in the north and Mozambique in the south, and that is slowly breaking Africa apart (figure 5.2). The Red Sea, which separates Africa from Arabia, formed as part of this process. Within Africa, the rift begins at the ‘Afar Triple Junction’ in Ethiopia – so called because one arm extends north-west up the Red Sea, one arm north-east along the Gulf of Aden (south of the Arabian Peninsula), and one arm due south into Africa.2 The rift runs south through Ethiopia and then – roughly around northern Kenya – divides into two parallel branches: to the east it forms the Gregory Rift, commonly known as the Eastern Rift or simply Rift Valley; to the west, the Albertine Rift.3 In Kenya, the Eastern Rift is Red Sea

Afer Triangle

Oubangui River

Congo Basin

Eastern (Gregory) Rift

Congo River Indian Ocean Albertine Rift

Figure 5.2. Map of the Rift Valley and the Congo Basin. Elevation is shown from light grey (low elevation) to black (high elevation), with the larger rift valley lakes shown in white. The broken white lines show the boundaries of the rift valleys. The solid black lines show the Congo River and its northern tributary, the Oubangui River.

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spectacularly developed, its flanking highlands giving way dramatically to the valley floor and yielding panoramic vistas. In Ethiopia, these highlands are even more precipitous, in places rising to well over 1 000 metres above the valley floor. The Albertine Rift is in many ways just as impressive as its eastern counterpart, but generally not as obvious or well known. For one thing, the highlands flanking the valley floor do not rise as steeply as in the Eastern Rift. For another, the blanket of rainforest under which it lies makes it difficult to find good vantage points, and hence decent views; the vegetation of the Eastern Rift, in contrast, is typically much sparser and drier. The Albertine Rift follows the borders between, to the west, the Democratic Republic of the Congo (DRC), and to the east (from north to south), Uganda, Rwanda, Burundi and Tanzania. Towards the south of Tanzania, the Albertine Rift and Gregory Rift – the eastern and western branches of the Great Rift Valley – converge once again to form Lake Malawi, before this huge fissure in the continent peters out in Mozambique. Along the entire length of its valley floor are large natural lakes, including Naivasha, Nakuru and Natron (Eastern Rift), and Tanganyika, Albert, Edward and Kivu (Albertine Rift). Eventually, some ten million years from now, this valley floor will drop below sea level and become flooded to form a sea similar to the one that currently separates Africa from Arabia. Note that Lake Victoria – the largest lake in the region, indeed in the whole of Africa – does not owe its formation to the Great Rift Valley. This much shallower water body was formed much later (some 400 000 years ago), when an up-thrown block in the Earth’s crust caused the damming of westward-flowing rivers. How does all this affect the distribution of Africa’s mammals? Remember that mountains and rivers act as barriers, as do changes in climate and vegetation. All four factors come into play in the Great Rift Valley. As a result, some species, particularly small terrestrial mammals, occur on one side of the rift but are absent from identical habitat on the other side. For example, the Gambian sun squirrel (Heliosciurus gambianus) occurs widely in west and south-central Africa but is curiously absent to the east of the Eastern Rift Valley. In contrast to the five other species in its genus, all of which are associated with some type of forest, this is a savanna species, with an unbroken distribution from Senegal in the west to Kenya and Ethiopia in the east.4 Yet in east Africa, it is confined to woodlands and savannas in western Ethiopia and in north-western Kenya, west of Lake Turkana. In other words, it has not made its way across the Eastern 104

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Rift. It might seem bizarre that such a widespread species, which ranges over thousands of miles of savanna, could be stopped in its tracks by a ‘little’ valley, but this nicely illustrates the influence of topographical barriers on species distributions. In other cases, the rift has divided populations of a species on either side of it, isolating them from each other. This has triggered speciation, with closely related species replacing each other on opposite sides of the valley. An example comes from wood mice of the genus Hylomyscus (figure 5.3) that are associated with forested habitats across tropical Africa. These rather cute little rodents have long tails and an opposable fifth digit of the hindfoot, which allow them to climb nimbly and thus forage in the understorey vegetation of forests. Most species occur in the main equatorial forest zone that includes the Congo Basin and the Upper and Lower Guinea forests. However, the species also occurs in forest pockets of east Africa such as the Eastern Arc forests of Tanzania. In Kenya, the genus occurs on both sides of the Eastern Rift and these two separate

Figure 5.3. A wood mouse (Hylomyscus simus), Sierra Leone. Photograph by Ara Monadjem.

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populations were long thought to represent a single species, Hylomyscus denniae. However, a taxonomic revision of this group, including a thorough study of the genetics of various east African populations by Terry Demos and his colleagues, showed that two separate species were involved. The population to the west of the Eastern Rift was identified as a new, previously undescribed species, Hylomyscus kerbispeterhansi, while the population on the eastern side proved to be H. denniae (Demos et al. 2014).5 Although these two species are similar in external morphology – and hence were previously thought to be one and the same – they are not each other’s closest relatives, and in fact belong to different species groups within the genus.6

HOTSPOTS To ecologists and evolutionary biologists – as opposed to night-clubbers or those seeking free Wi-Fi – a ‘hotspot’ is an area with an unusually high concentration of biodiversity. The Albertine Rift may well prove to be the hottest hotspot on the entire continent of Africa. If we are chasing impressive species totals or searching for zones of high endemism, we could do worse than focus on this region of prolific natural riches. For example, more than 700 species of bird have been recorded in the Virunga National Park, situated in the northern part of the Albertine Rift. This is more than the national totals for many African countries, and does not even include the many additional species that occur in the southern part of the Albertine Rift! In a recent analysis of bat richness on the African continent, the researchers showed that the Albertine Rift was predicted to support 80 species or more within a hectare of forest (Herkt et al. 2016).7 This rivals the richness of the Amazon Forest, making the Albertine Rift of importance not only on a continental scale, but also on a global one. Given the importance of the Albertine Rift, why is it that so few people have heard of it? Of course, ecologists and conservationists are well aware of the region’s riches but to the broader public they remain little known. There are several reasons for this. For a start, the region has suffered decades of instability, with regular warfare and civil turmoil discouraging visitors and engagement from the outside world. Also, the fauna, though richly diverse, comprises largely furtive, forest-dwelling species that are generally hard to observe, and not the conspicuous big-game herds and large, visible predators known from 106

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savanna habitats further east. In short, except for gorilla- and chimpanzeetracking in a handful of closely controlled locations, the Albertine Rift is not ‘safari country’ and thus does not attract the attention and resources lavished on Africa’s more accessible conservation areas. Whatever the reasons, this unique hotspot urgently needs far more visibility and support than it currently receives. Another continental hotspot for species diversity is the Upper Guinea rainforest in west Africa. This zone, which stretches from Ghana in the east to Sierra Leone in the west, was once carpeted in tropical rainforest – until the last century, when most of this was felled by humans, either for timber or to clear the land for agriculture and mining. Interestingly, it is separated from the Lower Guinea forests, which cover Gabon, the Democratic Republic of the Congo, the Congo Republic and the southern parts of Cameroon and Nigeria, by a narrow strip of savanna – corresponding to the two small west African countries of Benin and Togo – known as the Dahomey Gap.8 This break in forest cover has effectively isolated the Upper Guinea rainforest, encouraging local divergence and speciation that is reflected in the region’s numerous endemic taxa. Much of the Upper Guinea rainforest lies at low elevations, mostly below 500 metres above sea level. However, a few important mountains rise above this and have played a vital role in the processes that generate and maintain the region’s high biodiversity. Mount Nimba serves as an ideal example of such a mountain and is one I would like to discuss further – particularly since I have first-hand experience of it. Although covering only 670 square kilometres, this mountain straddles three countries: Liberia to the south, Guinea to the north and Ivory Coast to the east. In the north, it rises to 1 760 metres above sea level and is the region’s dominant geographical feature. Up until the early 1960s, the mountain was covered in rainforest – except the highest slopes, which are grassland (figure 5.4) – but much of this original forest has been either cleared or disturbed, mostly by ironore mining and slash-and-burn agriculture. The Albertine Rift may have the highest predicted diversity of bats in Africa – by which I mean the highest diversity that scientists would expect to find based on theoretical modelling – but currently Mount Nimba holds the record for the greatest number of bat species known to occur at any one spot: 59 species, all told. To put this in perspective, around 40 species of bats are known from the Kruger National Park in South Africa, an area 30 times larger, and far better surveyed, than Mount Nimba. And we have not yet recorded all Nimba’s species. In 2010, when I started 107

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Figure 5.4. Mount Nimba, showing the grassy slopes at higher elevations. Photograph by Ara Monadjem.

visiting this mountain, 41 species had been carefully documented and identified by 4 previous surveys in the 1960s and 1970s. We have since added 18 more species (Monadjem et al. 2016), of which 4 were new to science.9 Future studies will undoubtedly add even more.

FINDING REFUGE FROM A CHANGING CLIMATE We have seen how Mount Nimba is an important biodiversity hotspot for bats. However, its importance goes well beyond that. To appreciate just how far, we need to familiarise ourselves with the concept of ‘refugia’ (explained below), which, in turn, requires us to understand how Africa’s forests have reacted to changes in climate over the past two million years or so. I have mentioned in earlier chapters that Africa’s climate and hence its vegetation has not remained constant over evolutionary time. In fact, the climate has fluctuated widely. Although we are able to reconstruct the history of the planet’s climate over 108

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millions of years, we do not yet fully understand the reasons for its fluctuations; in any case, this complex subject requires a book of its own. We know, however, that ice ages have come and gone at regular intervals over the past two million years, with an average periodicity of about one in every 100 000 years. An ice age, in fact, comprises two very different periods: a long period of cold weather, called a glacial; and a much shorter period of balmy weather, called an interglacial. We are currently in an interglacial. However, 18 000 years ago we were at the height of a glacial, and this period was called the Last Glacial Maximum (LGM). In fact, this glacial extended from about 120 000 to 12 000 years ago. Hence, the entire history of ‘civilised’ humanity (that is, since the advent of agriculture) is restricted to this latest interglacial that we currently find ourselves in. Ice ages, as the name suggests, are all about the expansion and contraction of vast sheets of ice centred on the two poles. At the LGM – their greatest extent – these ice sheets would have reached the latitudes of modern-day Chicago in North America and Oslo in Europe. This, as you can imagine, would have had severe consequences for the fauna and flora of northern latitudes. The ice sheets did not reach Africa, at least not during the past two million years, but the continent was not spared the mayhem of an ice age. The changes it brought about had more to do with rainfall than temperature. As more of the Earth’s free-standing water became locked up in ice, less of it was available to fall as rain. In consequence, much of the region’s forests were converted to grasslands and woodlands – only to revert to forest during the following interglacial. In other words, Africa’s forests have regularly expanded and contracted in step with the expansion and contraction of the ice sheets. Hence, the tropical forests of the Congo Basin and the Lower and Upper Guinea forests as we now know them offer just a current snapshot of the region. During the LGM, much of this zone was covered either by grassland or by a woodland–savanna mosaic, not the rainforest that carpets it now – or that would do, if we hadn’t chopped it down. This conclusion is not just mere supposition based on fancy computer-generated models: meticulous study of ancient pollens from sediments in the region has provided solid evidence for this hypothesis (Maley 1991; Maley and Brenac 1998). Forest refuges How would mammals have responded to such changes? This would have depended to some extent on the type of mammal. Some species, no doubt, 109

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would have adapted behaviourally and physiologically to the changed landscape, but essentially stayed put. This is probably true of chimpanzees and other more adaptable forest species that we associate with tropical forest but are able to survive in forest–woodland mosaics. In south-eastern Senegal, for example, chimpanzees live in savanna hundreds of kilometres from the nearest tropical forest (Pruetz et al. 2015). Other species may have tracked the forest in their distributions, disappearing when it contracted and reappearing when it subsequently expanded again. This might have been the case with gorillas and other more inflexible forest-dependent species (Xue et al. 2015). Tracking forest as it ‘moves’ across the landscape is perhaps not the best way to view the process. Individual animals are unlikely to have been able to travel far in order to reach suitable areas of habitat. Instead, it is likely that some of those individuals that lived in areas where the forest persisted would have survived the glacial and subsequently seeded the populations that bloomed when forests expanded again during the warmer and wetter interglacial. This pattern would explain the rather curious distribution of gorillas, which occur in two main populations (figure 5.5): the western gorilla (Gorilla gorilla) is sandwiched between the Oubangui and Congo rivers to the east and south, and the Sanaga River to the north (covering Gabon, the Congo Republic and southern Cameroon); the eastern gorilla (G. beringei) is packed between the Lualaba River and the Albertine Rift (eastern DRC, western Uganda–Rwanda).10 In other words, there is a 1 000-kilometre gap in their distribution smack-bang in the middle of the Congo forest – an area of apparently suitable habitat that is teeming with chimpanzees but devoid of any gorillas. Interestingly, these two gorilla populations, which are sufficiently divergent to represent distinct species, separated more than a million years ago but maintained genetic contact right up until about 20 000 years ago, coinciding with the LGM. It would appear that gorillas were holed up in two separate populations during the last glacial when forests had contracted, but have not expanded during the interglacial that we find ourselves in now – and, given their precarious conservation status, probably never will. So, where exactly did Africa’s forests retreat to during glacial periods – or, put another way, where were the patches that survived? There is evidence that the same regions served as the last remaining pockets of forest at the peak of each ice age. These areas would not only have been vital for the continued existence of forests but also served as refuges for all the organisms that we know inhabit them today. They are thus known as ‘refugia’ (singular ‘refugium’). The 110

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Oubangui River

Gorilla beringei Gorilla gorilla

Congo River

Atlantic Ocean

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Figure 5.5. Map of the distribution of the two gorilla species Gorilla gorilla (stippled) and G. beringei (grey shading). The Congo and Oubangei rivers are shown as thick black lines, with the Oubangei branching to the north. Note the absence of gorillas in the forested region in between.

distribution of gorillas suggests that the Albertine Rift and the Lower Guinea forests served as just such refugia. In fact, there is close correspondence between the pattern that we see with gorillas and many other groups of mammals – and even with birds, which we normally categorise as good dispersers because of their powers of flight. A study by Irina Levinsky and her colleagues modelled the anticipated distribution of birds and mammals during the LGM, based on what we deduce the climate would have been like during that period (Levinsky et al. 2013). Using this method, the researchers located six areas that potentially served as refugia for birds and mammals. Three of these areas are of interest to us in relation to tropical rainforest: the Upper Guinea rainforest, the Cameroon–Nigeria highlands and the Congo Basin. Their analysis did not specifically identify the Albertine Rift as a refugium. Earlier studies of current bird distributions, however, have recognised the Albertine Rift (Fjelda and Lovett 1997), so it remains unclear exactly what the role of this region was during the LGM. 111

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Desert refuges The role of forests as refugia is well established. But there are also refugia at the other end of the habitat continuum: the arid zone. Being humans, we naturally associate rain and lush vegetation with a productive and healthy environment. When we learn that the Sahara Desert was once woodland, we see this as a positive thing – and so it was for humanity: our ancestors grazed livestock and raised crops in what is now pure sand desert. However, we would not feel that way if we were desert-adapted creatures. For such beasts – the likes of camel or oryx – a forest represents an unwelcome intrusion into their normally parched landscape. The jerboas of the genus Jaculus (family Dipodidae) provide a good example. These curious little rodents, weighing barely 30 grams, have comically large ears and eyes, a long tail ending in a black tuft, greatly reduced forelimbs and long, slender hindlimbs, on which they proceed using bipedal, kangaroo-like hops. Jerboas occur throughout north Africa and across Arabia to Mongolia, although members of the genus Jaculus do not extend beyond Pakistan. Three species inhabit North Africa.11 One, J. orientalis, is restricted to the Mediterranean region, hugging the coastal zone. Two species occur further south in the Sahara Desert, with J. jaculus occurring throughout the region and J. deserti restricted to the north-western part of Africa from Tunisia to Mauritania. These latter two species are indistinguishable on anatomical or even chromosomal grounds; the only way to distinguish them is through molecular analysis.12 But the large genetic divergence between them leaves no doubt that they represent distinct species (Boratynski et al. 2012). Furthermore, and perhaps more interestingly, another genetic study has shown that the two species have radically different pasts (Ben Faleh et al. 2012). Whereas the widespread J. jaculus has a long history of expansion and contraction in the region, J. deserti only expanded its range as recently as 20 000 years ago, coinciding with a dry period. It seems that as the Sahara became more lush and vegetated, the jerboas contracted their ranges into small, isolated arid refugia, enabling J. deserti to diverge genetically from the parental J. jaculus. On subsequent aridification, the two species expanded their ranges and eventually overlapped each other (but maintaining their individual species boundaries), the pattern that we see today. Another example may help to clarify the role of refugia in arid environments. Earlier in this chapter I described how the major ecological discontinuity of the African continent has traditionally been seen as that between the savannas of 112

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southern and east Africa and the forests of central-west Africa. In fact, this may not be entirely accurate. The orientation is fine, but the habitats are not. For example, at diagonally opposite ends of the north–south zone are two deserts in Somalia–Ethiopia and Namibia–Angola, respectively. To call this a savanna zone, therefore, is not technically correct. In a similar fashion, the broad swathe of tropical forest in the east–west orientation is bordered to the north by the Sahel, an equally broad swathe of woodland and savanna. Again, calling this the forest belt is not correct. Because of the north–south orientation of the ‘savanna’ zone, the two arid regions are discontinuous and examining their mammals is rather instructive. This is because many mammal species occur in both these zones but are absent from hundreds of thousands of square kilometres in between. Take the bat-eared fox (Otocyon megalotis). This adorable, bushy-tailed little canid is insectivorous, using its large ears to locate subterranean insects, which it then digs up using its paws. It is widespread in savanna regions of east Africa, occurring in southern Ethiopia, Somalia, Kenya and Tanzania. However, it then ‘skips’ across Zambia, Malawi, the southern DRC and Mozambique to reappear in similar habitats across Namibia, Botswana, western Zimbabwe and western South Africa. Why is it absent from the vast areas of savanna in between? The answer is that not all savannas are ‘equal’. In crude terms, African savannas fall into two types: a mesic, nutrient-poor, broad-leafed savanna called miombo woodland, and an arid, nutrient-rich, fine-leafed savanna dominated by acacia trees. The bat-eared fox lives in the latter but completely avoids miombo woodlands. These two discrete populations would have been continuous (or nearly so) during cool, dry glacial periods, but have become totally isolated during the current interglacial. This peculiar distribution of the bat-eared fox is echoed in that of many mammal species and other vertebrates. Some taxa are represented by distinct species on either side of the divide, such as the gemsbok (Oryx gazella) and east African oryx (O. beisa), thus demonstrating that these lineages have been separated for a long time. Others are represented by subspecies, such as those of the bat-eared fox and black-backed jackal (Canis mesomelas, figure 5.6), which indicates more recent genetic exchange between the two regions. Still other taxa have radiated in one region but not in the other, indicating that they reached the second region more recently. This is shown by the dik-diks of the genus Madoqua, which are among Africa’s smallest antelopes, barely larger than a hare, of which four species occur in east Africa but just one in Namibia–Angola. With all these mammal species, the explanation for their occurrence at opposite 113

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Figure 5.6. A black-backed jackal (Canis mesomelas), Kruger National Park, South Africa. Photograph by Ara Monadjem.

ends of the savanna zone has to do with the climate-mediated contraction and expansion of these arid zones. During cool, dry glacial periods these arid zones expanded at the expense of the miombo woodlands, which ‘moved’ to occupy the space vacated by rainforest. An arid corridor must have developed, which allowed these mammals to move between the two areas.

THE IMPORTANCE OF MOUNTAINS We have seen that as climate changes, so does vegetation, resulting in a complex process of expansion and contraction of forests and arid zones over millennia. Animal populations track these changes, at times contracting their ranges to refugia, at other times expanding to cover larger areas of the continent. In the process, isolated populations in refugia may occasionally diverge sufficiently from populations in other refugia to give rise to new species. Hence, refugia play a fundamental role in ensuring the long-term persistence of species and serve as ‘species pumps’, by encouraging the process of speciation. 114

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So, what distinguishes these refugia? Are there any geographical characteristics common to them all? There does seem to be one particular feature that is regularly associated with refugia, and that is mountains. This makes good ecological sense, as mountains add considerable variability to the climate of a region. To see how this works, let us imagine a continent without any mountains: essentially a flat landscape stretching from the equator away to the south or the north – the direction does not matter. The climate at the equator is typically hot and wet. As we move away from the equator, the average annual temperature and humidity drop. But we have to move hundreds of kilometres away to experience a biologically meaningful drop. Maputo, for example, at latitude 26° south is several thousand kilometres south of Mombasa, which is very close to the equator, yet the drop in temperature is relatively small and probably not noticeable except on winter nights. Now, instead of moving away from the equator, imagine we remain near it but instead climb up a mountain – say Mount Kenya. As we gain elevation, we feel the temperature dropping. A moderately fit person could start the day in tropical heat at the base of the mountain and end it in cool temperate conditions at 3 000 metres above sea level. By the next day, the person could be at the summit, 5 199 metres above sea level, and experiencing sub-zero temperatures! My point is that an ‘easier’ way for an organism to escape the loss of its habitat, as this habitat contracts across the landscape, is to follow it up or down a mountain. The effect on a forest habitat of movement across a distance of several hundred kilometres on flat ground could, in theory, be accomplished by an elevational change of just a few hundred metres on a mountain. And it is not only temperature that changes as you climb a mountain. Mountains, by their nature, tend to trap clouds, which results in heavier rainfall. Therefore, mountains in tropical zones must have served as important refuges for forest species as lowland forest habitats contracted during dry periods. Furthermore, small pockets of forest on isolated mountains probably served to encourage speciation, adding to the subsequent biodiversity of the zone. It is for this reason that mountains such as Mount Nimba are critically important biodiversity areas – not only because of their very high species richness, but also because they serve as refugia.

RIVERS AS BARRIERS Rivers act as formidable barriers to terrestrial animals. They even deter many birds – especially smaller, furtive species that avoid open spaces. This is not 115

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always intuitively obvious to humans, who for thousands of years have been navigating open waters in canoes and rafts. But remove the floating object, and a 2-kilometre stretch of open water becomes impassable to 99 per cent of us. Now, add to the mix a strong current, turbulent water and hungry crocodiles, and the proportion of humanity that can safely cross the river declines sharply – perhaps right down to zero. Africa has several large rivers that fit this bill, and have played an important role in shaping mammalian communities by reducing or preventing movement across the landscape. Among the most important, and impressive, are the Niger, Congo, Nile and Zambezi. These are truly daunting rivers. As the longest river on Earth, the Nile is perhaps the best known. However, it is the Congo, which has the second largest discharge rate of any river after the Amazon River, that is most significant from a biogeographical perspective, and this is the river we will consider further here. The Congo River is some 4 700 kilometres long and, remarkably, almost entirely confined to the Democratic Republic of the Congo, the huge country that bears its name. Although the river’s source is actually the Chambeshi River in northeastern Zambia, and some of its other tributaries originate in northern Angola and the Central African Republic, for the most part this mighty river flows within the border of the DRC, in places forming national boundaries with the Republic of Congo and Angola. Various tributaries enter the Congo at different points, including the Lualaba, Lomani, Oubangi and Kasai. Each of these is a major river in its own right, and we will see later in this chapter the impact they have had on the distribution of small mammals. But let’s start with the Congo itself. This river has been running the same course for about 34 million years (Takemoto et al. 2015), which is a very long time, given the frequency with which rivers ‘capture’ other rivers and, as a result, change direction. The upper part of the Zambezi River, for example, once flowed into a vast palaeo-lake that covered much of northern Botswana, south-western Angola and even parts of the Congo Basin, but was captured by the middle Zambezi and now drains eastwards into the Indian Ocean in Mozambique.13 All this happened in the past two million years – and, as you can imagine, has had interesting implications for the evolution of fish in the region. The relationship between great apes and rivers You would expect a 34-million-year-old barrier like the Congo River to have had a profound impact on the region’s mammals, and indeed it has. There are 116

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very many examples of this, but since we have been talking about the great apes we will focus on them here. All gorillas occur only north of the Congo River, despite there being plenty of suitable habitat south of it. Hence, the Congo has been an absolute barrier to gorillas. What about chimpanzees? Here we see a different story. There are chimpanzees on both banks of the river, but they belong to different species (figure 5.7). On the right (north) bank, we find the common chimpanzee (Pan troglodytes), while on the left (south) bank, we encounter the bonobo (Pan paniscus) – sometimes also called the pygmy chimpanzee, which is misleading as this species is no smaller than its northern cousin.14 These two apes are morphologically distinct and exhibit very different social and behavioural traits. The bonobo is a slenderer species than the common chimpanzee, with longer limbs, narrower

Sanaga River

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Pan troglodytes verus Pan troglodytes ellioti

Pan troglodytes troglodytes

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Pan troglodytes schweinfurthii Pan paniscus

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Figure 5.7. Distribution of chimpanzee species in relation to river barriers in west Africa. Note how the large rivers Sanaga, Congo and Oubangui form the borders of the species or subspecies of chimpanzees, attesting to the importance of rivers as barriers to African terrestrial mammals. Pan paniscus is the bonobo, while Pan troglodytes verus, Pan troglodytes ellioti, Pan troglodytes troglodytes and Pan troglodytes schweinfurthii are subspecies of the common chimpanzee Pan troglodytes.

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shoulders and a smaller head, and is born with a  dark rather than a pink face. Its communities also maintain a more matriarchal social structure, with an emphasis on social bonding rather than conflict, and relationships reinforced through frequent sexual contact (sex being known as the ‘bonobo handshake’). The differences between the two species are hardly surprising, given that they diverged between one and two million years ago. But how did their ancestors cross the river? A recent study suggests that the Congo was too serious an obstacle during this period to have allowed ancestral bonobos to cross it (Takemoto et al. 2015). Instead, the authors of this study have argued that chimpanzees may have crossed around the upper reaches of the Lualaba River, far to the south of their current range. This would have required them to survive outside their normal rainforest retreat, but – as we have seen already – chimpanzee populations are capable of adapting to a savanna habitat. After crossing the Lualaba River, the chimpanzees would then have had to travel northwards in order to reach their current distribution, which presumably they did by retracing their steps, but on the opposite bank of the river. The relationship between chimpanzees and rivers does not end here, though. The common chimpanzee, on the right bank of the Congo, occurs in a moreor-less continuous swathe from Uganda in the east to Nigeria in the west. The species is absent from the Dahomey Gap, but makes a reappearance in the Upper Guinea rainforest. It should not surprise you, then, to learn that the Upper Guinea population has diverged sufficiently from other common chimpanzee populations to warrant recognition of its subspecies status.15 But it might surprise you to learn that within the continuous range of the chimpanzee, from Uganda to Nigeria, there are three subspecies, each neatly delineated by a large river. The Oubangi River, a large tributary of the Congo, separates the eastern and central chimpanzees, while the Sanaga, a large river running through central Cameroon, separates the central chimpanzees from Elliot’s (or Nigerian) chimpanzees (Bjork et al. 2011). Now consider what this means. A chimpanzee standing on the eastern side of the Oubangi River is genetically more similar to chimpanzees in Uganda, more than a thousand kilometres away, than it is to those standing on the opposite bank of the same river, and quite possibly even within eyeshot or earshot. The same is true on the banks of the Sanaga River. This is clear evidence of my claim that rivers are formidable barriers to terrestrial mammals. .

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River barriers to small mammal movement So far, we have looked at the impact of rivers on the distribution of relatively large mammals, but what about smaller animals such as rodents or shrews? Some of the best work on these mammals has been done on rivers in the Congo Basin, so we will stay in that region and consider Praomys, a diverse and abundant genus of rodents that comprises the soft-furred mice of tropical Africa (figure 5.8). Currently 16 species are recognised (Monadjem, Taylor et al. 2015), but several recently identified clades require naming and no doubt several species await discovery (Mizerovská et al. 2019). These delightful little creatures are covered in a coat of soft, silky fur, from which they derive their name. They occur throughout the Congo Basin, and well beyond into west and east Africa. An extensive study of Praomys species was conducted by Jan Kennis as part of his PhD thesis in Herwig Leirs’s lab at the University of Antwerp, Belgium.16 Kennis carried out his study on both banks of the Congo River at a large city called Kisangani, some 1 800 kilometres upstream from the mouth.

Figure 5.8. A west African soft-furred mouse (Praomys rostratus), Sierra Leone. Photograph by Ara Monadjem.

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He collected a large sample of 654 Praomys specimens and then exposed them to rigorous molecular analysis. This was the first detailed molecular study of the genus anywhere in the Congo Basin and the results were telling. Of the seven species he recorded from his study area, three were restricted to the left bank and three to the right bank; only a single species, P. mutoni, occurred on both sides of the river (Kennis et al. 2011). Interestingly, the species common to both banks is naturally associated with seasonally inundated habitats within tropical forest and may therefore be at home in water. This may have ‘pre-adapted’ it to making the Congo River crossing – a hypothesis that could perhaps be tested by examining how its swimming ability compares with that of other members of the genus. Such swimming tests have been conducted on other rodent species and, unsurprisingly, rats that inhabit swampy habitats are better swimmers than purely terrestrial rats (Nicolas and Colyn 2006). In contrast, the tributaries of the Congo did not serve to separate distinct genetic populations of Praomys. Thus, it seems, the mighty Congo River serves as a significant barrier to small mammals but its smaller tributaries probably do not – a pattern that is echoed in rivers in other parts of Africa (Jacquet et al. 2014; Nicolas et al. 2012).

THE AFROMONTANE REALM: MOUNTAINS AS ‘ISLANDS’ In 2003, the leading systematist and biogeographer Rauri Bowie completed a PhD thesis that he titled ‘Birds, Molecules, and Evolutionary Patterns among Africa’s Islands in the Sky’ (Bowie 2003). By ‘islands in the sky’, he was, of course, referring to mountaintops. Bowie’s focus was on the Afromontane zone, a highly discontinuous ecoregion that extends, in fragmented sections, from Ethiopia in the north right down to South Africa, with isolated peaks in west Africa. Since all these mountaintops have vegetation that is similar, but radically different from the vegetation found at lower elevations, these peaks are effectively islands for the species that inhabit them. Typically, the higher peaks are covered in lush grassland and heathland, while the lower slopes are dominated by woodland or forest, grading into savanna at the bottom. A grassland-adapted rodent such as a vlei rat (genus Otomys) may thus find the grassy glades of the plateau most agreeable, but will not set one foot in the surrounding forest. Such species are trapped on mountaintop islands, surrounded by a sea of inhospitable forest and savanna. 120

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How, then, do vlei rats move between mountains? This question has been the life’s work of Peter Taylor, from the University of the Free State in Q ­ wa-Qwa, South Africa (figure 5.9). Among much other research of the highest calibre, he has dedicated a quarter of a century to Otomys. One of his great achievements has been a thorough revision of the genus, which has resulted in the recognition of 31 species – as of 2015, when he and I published our book, co-authored with Christiane Denys and Woody Cotterill, Rodents of Sub-Saharan Africa (Monadjem, Taylor et al. 2015).17 Not only did he convincingly demonstrate that many cryptic species had been overlooked, he also showed that our understanding of their evolutionary relationships had been, for the most part, completely wrong. The reason for this lay in our old friend, convergent evolution. The scattered montane habitats in which Otomys species occur

Figure 5.9. Peter Taylor removing a rodent (not visible) from a Sherman live trap in northern South Africa. Photograph by Ara Monadjem.

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have exerted similar evolutionary pressures on this group, moulding species in similar habitats into similar ‘morphotypes’. Hence, before the advent of molecular sequencing, when systematists created evolutionary trees based on anatomical features – in the case of mammals, these were mostly cranial and dental characteristics – the species of Otomys that shared similar morphologies were lumped together as closely related. By applying molecular techniques, combined with a painstaking anatomical study of hundreds of specimens, Taylor and his colleagues have made great strides in resolving the relationships between many taxa of the genus Otomys (Taylor et al. 2019, 2014, 2011). Some idea of how Herculean a task this was is evident from the length of their landmark 2011 paper, which ran to 66 pages – the length of a short book. To illustrate what we have learnt from studying the genus Otomys, we can turn to Mount Elgon, on the Uganda–Kenya border (figure 5.10). The summit of this extinct, cone-shaped volcano towers 4 321 metres above sea level. Three Otomys species occur on the mountain. At mid elevations, some 2 400 to

DR CONGO

Mt Elgon (4 321 m)

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Lake Albert Ruwenzori Mts (5 109 m)

Lake Kivu

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Lake Edward

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Lake Victoria RWANDA

Mt Kilimanjaro (5 895 m)

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Figure 5.10. Map showing location of Mount Elgon in relation to other high east African mountains. Note the isolated nature of these uplands (shown in darker colours, with black shading indicating areas above 3 200 metres), which gave rise to the ‘islands of the sky’ moniker.

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3 000 metres above sea level, there is a belt of Afromontane forest and bamboo just below the grassland, which is the haunt of Otomys tropicalis. Above this elevation, where the trees give way to grasses, we find two other species: O. jacksoni and O. barbouri. What makes the study conducted by Taylor and his colleagues so interesting is that, prior to their work, O. jacksoni (under the name O. typus) was thought to be widespread on mountaintop grasslands in east Africa. Therefore, the closest relatives of O. jacksoni, based on anatomical studies, were conjectured to be those on other high mountaintops, including Mount Kilimanjaro, the Ruwenzori Mountains and the Ethiopian highlands. Taylor et al.’s molecular studies, however, revealed that the closest relative of O. jacksoni is O. tropicalis, the species that occurs in the bamboo belt at elevations immediately below it. The third species, O. barbouri, is unrelated to the other two and represents an independent colonisation event. The same pattern shows up on other mountains, where the closest relatives of the species of Otomys occupying the montane grasslands near the top are those species living in the forested belt below. Not only is this a wonderful study for explicating relationships and delineating species boundaries; it also makes it easier to provide a meaningful biogeographical setting. We do not have to explain how a montane grassland species managed to colonise distant mountaintops by travelling over vast tracts of inhospitable savanna and forest. The woodland species did the moving – tracking their habitat during periods of contraction and expansion, as we discussed earlier – and then gave rise to the grassland species in situ. Science tends to be more beautiful whenever the explanation is simpler! So, what happened to the roan and sable antelope I introduced at the start of this chapter? Why is the roan antelope distributed widely across the savannas of Africa on both sides of the equator, while the sable antelope is limited to savannas south of the equator? We don’t yet know the answer to this question, but based on what we have learnt in this chapter we can speculate as follows. Sable and roan (genus Hippotragus), together with oryx and addax, are members of the tribe Hippotragini (Hassanin et al. 2012). As I explained in chapter 1, oryx and addax are arid-adapted antelope and it would appear that all members of this tribe evolved from an arid-adapted ancestor, with a Eurasian origin (Hassanin et al. 2012; Kingdon and Hoffman 2013). This would suggest that ancestral Hippotragus species invaded sub-Saharan Africa from the north. The roan and sable lineages split perhaps 8.5 million years ago, while roan and blue antelope 123

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(the extinct South African species) split more recently, around 2.5 million years ago (Hernandez-Fernandez and Vrba 2005). Putting all these pieces together, I would hazard a guess that the ancestor of the roan and sable antelopes once roamed the arid savannas of north Africa, but shunned the lush rainforests of the Congo Basin, and was thus effectively cut off from the southern savannas. At some point around 8.5 million years ago, a small population found its way across from the northern savannas into east Africa (perhaps through modern Uganda, during a period of cooling and forest contraction), and became the ancestor of the sable antelope. Populations north of the equator evolved into the roan antelope, while those to the south gave rise to the sable antelope. Much later, the roan antelope managed to cross the divide, perhaps using the same route as the ancestral sable antelope had done millions of years earlier, allowing roan to colonise the southern savannas. Today, unlike their ancestors, neither roan nor sable antelope are arid-adapted; they are closely tied to mesic savannas such as miombo woodland, where they avoid both competition with plains antelopes (particularly the wildebeest and hartebeest of the sister tribe Alcelaphini) and predation by lions. The blue antelope, which was restricted to low-nutrient landscapes of the southern regions of South Africa, then evolved from a stock of roan antelope that had somehow become geographically isolated to the south. *** In this chapter, we have examined the role of barriers in the movement of animals on the African continent. We have identified four main types of barrier – climate, vegetation, rivers and mountains – and looked at interactions between them. Barriers have been critical in preventing certain mammals from reaching suitable habitat, thus explaining the absence of species from otherwise ideal locations. They have also served to separate populations of the same species, and over time have led to divergence and speciation. These biogeographic processes take place over long periods of evolutionary time. In the next chapter, we will focus on processes that affect the distribution of species over much shorter, ecological time scales.

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or at least two hundred million years our planet was dominated by organisms so massive that modern elephants look quaintly diminutive by comparison. Lumbering sauropods, weighing dozens of tons, roamed Earth as Pangaea fractured and the fragments drifted apart, eventually forming the continents we are familiar with today. Argentinosaurus, for example, was more than 30 metres in length and is estimated to have weighed 73 tons (Mazzetta et al. 2004). The end-Cretaceous mass extinction that took place 66 million years ago saw the complete disappearance of all these giant dinosaurs, but the resulting vacuum was quickly, in evolutionary terms, filled by mammals. Previously, the largest mammals had weighed less than 10 kilograms (little more than a domestic cat), but in less than 25 million years there were species weighing 10 tons – double the size of a large savanna elephant. Thus, by 40 million years ago, our planet was once again home to enormous creatures, but this time they were mammalian, rather than dinosaurian/reptilian, in nature. Considering the very long relationship that megafauna have had with our planet, you might imagine that they have played an integral role in shaping and maintaining its terrestrial ecosystems. And you would be right. Only now are we beginning to piece together the critical functions that megafauna provide – or, more correctly, provided, since sadly most of these huge animals are no longer with us. To understand why this is so, we need to look at human history, particularly the happenings of the past 50 000 years.

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HUGE MAMMALS OF THE PAST: EXTINCT MEGAFAUNA What exactly do we mean by ‘megafauna’? The term typically refers to any large terrestrial animal weighing more than one ton (N. Owen-Smith 1987; R.N. Owen‐Smith 1992). In fact, the term ‘megaherbivore’ was coined by Norman Owen-Smith, a brilliant ecologist, now retired from the University of the Witwatersrand in Johannesburg, South Africa. I was lucky enough to complete my master’s degree under his supervision but, unhappily, did not study his key papers until many years later. Today, megafauna encompass just four groups of terrestrial mammals: elephants, rhinoceroses, hippopotamuses and giraffes. But giant mammals abounded until recent times – recently enough for our species to have encountered them – and included many other groups. Some of these vanished giants were many times larger than the largest extant megafauna.1 The savanna elephant, the planet’s largest terrestrial mammal today, occupied a humble 12th position 50 000 years ago, and was barely one-third the weight of a Deinotherium, a genus that died out at the beginning of the Pleistocene epoch (about two million years ago).2 The list of recently extinct megafauna includes several other groups. In South America, these included the giant sloths, a diverse group of South American mammals related to today’s sloths (order Xenarthra) that included at least 18 species weighing more than a ton. On the same continent, you would also have encountered the notoungulates and litopterns, two orders of large mammals that resembled the hoofed ungulates found on other continents, and whose systematics have been the subject of much debate. Though some scientists have suggested a link to Africa’s Afrotheria (see chapter 3), more recent work based on collagen tissue extracted from ancient bones supports a sister relationship with the order Perissodactyla, which comprises today’s horses and rhinoceroses (Buckley 2015). Either way, at least six species belonging to these two extinct orders could be considered megafauna. And then there were the Diprotodontia, restricted to Australasia. Today we are all familiar with diprotodont marsupials, as they include kangaroos, but this order also once included two species of the genus Diprotodon that were as big as a small rhinoceros. These creatures even resembled rhinoceroses, albeit ones without horns, but the two groups do not share a recent ancestry and must have evolved their similarities through convergent evolution. 126

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Among the ranks of megafauna some 40 000 years ago there were also, of course, many types of elephant (order Proboscidea; 14 species), even-toed ungulate (order Cetartiodactyla; 11 species) and odd-toed ungulate (order Perissodactyla; 7 species) (Koch and Barnosky 2006; Smith et al. 2003).3 Among the extinct even-toed ungulates were various oxen, bison, camels and elk that all reached greater sizes than their modern relatives. Today, the only even-toed ungulates to qualify as megafauna are the giraffes (Giraffa) and the hippopotamuses (Hippopotamus), with the common hippopotamus being the largest extant species, weighing up to two tons or more. The real giants of the Pleistocene, however, were the various groups of elephant and  rhinoceros. The extinct giant rhinoceros Paraceratotherium, which grazed the grassy plains of Eurasia, weighed up to an estimated 19 tons and towered 4.8 metres at the shoulder. This bizarrely put-together creature would have looked out of place among today’s rhinoceroses, having a long neck and no horns, but would certainly have been a spectacular sight. The largest land mammal yet discovered, however, was a proboscidean Palaeoloxodon, which had an estimated weight of 22 tons. Members of this extinct genus were closely related to the two extant genera of Elephas (Indian) and Loxodonta (African) elephants and, like them, had two large tusks. They originally evolved in Africa but subsequently colonised Eurasia. Palaeoloxodon appears to have become extinct in the Late Pleistocene, while Paraceratotherium became extinct some 20 million years ago, both long before humans roamed their native landscapes of Eurasia. Humans, however, would certainly have encountered the Columbian mammoth Mammuthus columbi, which weighed up to about ten tons, or twice the size of a large bull savanna elephant. These leviathans roamed the plains of North America until their disappearance around 11 500 years ago.4 Given that Africa has the vast bulk, so to speak, of today’s megafauna, we might be excused for believing that the continent has always been a focal point for these giant mammals. In fact, this is not the case. As we have seen, prehistoric megafauna were distributed across every major continent on the globe, including Australia. Indeed, a mere 20 000 years ago, Africa would have ranked second-last in terms of the abundance and diversity of megafauna, behind every other continent except Australia. During the Late Pleistocene, Africa had seven types of megafauna, of which four survive today: elephants, rhinoceroses, hippopotamuses and giraffes (figure 6.1). 127

(a)

(b) Figure 6.1. The four groups of megafauna alive today: (a) elephants, (b) rhinoceroses, (c) hippopotamuses and (d) giraffes. Photographs by Ara Monadjem.

(c)

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8 (4)

9 (0)

9 (4) 3 (4) 20 (0)

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Figure 6.2. The number of species of megafauna present in the Late Pleistocene with the number of species remaining today in parentheses. Based on Malhi et al. (2016).

By contrast, during the same time period, Australia, North America, Eurasia, South Asia and South America had, respectively, 1, 9, 12, 13 and 20 megafaunal representatives (Malhi et al. 2016). Within a few thousand years, at the very most, but probably within a few hundred years on most continents, this diversity had all but disappeared. Megafauna vanished completely from the Americas and Australia, and almost completely from Eurasia and South Asia (figure 6.2). Why did Africa have relatively few megafauna at the end of the Pleistocene? And what happened to the megafauna of the other continents? The answer lies with the first super-predatory mammal species ever to have inhabited this planet: Homo sapiens.

WIPING OUT THE MEGAFAUNA: THE IMPACT OF HUMANS There are many ways in which we humans could – and do – describe ourselves. These range from the highly critical (greedy, aggressive, superstitious, 130

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intolerant and so on) to the equally highly self-congratulatory (kind, generous, thoughtful, wise and the like).5 We could waste countless hours arguing the merits of each description and never reach unanimous agreement. Besides, such considerations belong in the realms of philosophy. From the perspective of evolutionary biology, however, there is one human attribute that nobody can deny: as a species, we have been supremely successful. I mean this in a nonvalue-laden way – I am not saying that our success is either a good or a bad thing, simply that it has come to be. We have learnt not just how to survive and thrive, but also how to manage our environment to our benefit, enabling us to colonise or utilise every last corner of the planet. We grow and store our own food; we harvest timber resources for manufacturing homes and furniture; we extract minerals from the bowels of the Earth to build cars, planes and boats; we produce and store our own energy; we manage or remove harmful species such as bacterial pathogens and predators; and we overcome our competition – which, unfortunately, includes other human beings. What’s more, we share what we have learnt with our children and fellow humans by way of language, books and digital communication, thus ensuring that our skills and knowledge are not only retained but also constantly improved. As a result, our global population has grown unchecked for millennia at rates unheard of for any other mammal – or perhaps even any other multicellular organism. Before I am misunderstood, let me make it clear that I am in no way implying that we have become the ‘Masters of the Universe’, somehow extricating ourselves from the delicate web of nature in order to preside over it. Neither am I implying that our success will necessarily continue into the future. I am simply contending that until the arrival of Homo sapiens, planet Earth had not encountered a species that was capable of such extreme domination. At any rate, once ‘modern’ (tool-wielding) humanity was unleashed on the planet there was little that could stop our progress. We evolved in Africa from Australopithecine apes, over a 6-million-year period. This was enough time for most of the other mammalian species with which we shared the continent to develop defensive strategies and behaviours, enabling them to avoid or reduce catastrophic extinctions. It may thus explain why only half of the African megafauna present in the Late Pleistocene became extinct: these animals had the benefit of having evolved alongside our ancestors and were thus able to adapt to their presence and develop ways to prevent easy capture. However, our African background may also explain why there were fewer megafauna at the end of 131

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the Pleistocene to start with: our immediate ancestor Homo erectus must have been a formidable predator, hunting with stone tools (and perhaps traps) and utilising fire to manage the ecosystem, and may have driven a few large mammal species to oblivion.6 We do not know this for sure but, considering what devastation Homo sapiens is capable of, I would not put it past Homo erectus to have been the culprit in at least some of those early Pleistocene extinctions. But let us return from the realm of speculation to what we do know about megafauna extinction and humanity. There is a close correspondence between the arrival of Homo sapiens on virgin lands (areas without humans) and the disappearance of all sorts of animals, including megafauna (Bartlett et  al. 2016; Koch and Barnosky 2006). This is best recorded on islands such as New Zealand and Tasmania, but also on large continents – especially North and South America. We know that climate has also played a role in these extinctions. However, remember that the climate over the past 2.5 million years (that is, during the Pleistocene) has involved some 17 glacial events (figure 6.3), resulting in massive fluctuations in temperature and rainfall. It

Figure 6.3. Map of the maximum extent of the ice sheets (grey shaded areas) during the last glacial event (18 000 years ago). Based on Batchelor et al. (2019).

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would therefore seem more than a little odd if megafauna had survived 16 of these ice ages but succumbed to the 17th, which was no more severe than any of the previous ones, without some other factor being involved. In any case, the disappearance of megafauna was not mirrored by similar levels of extinctions among smaller mammals. If we accepted that climate was the underlying cause of these extinctions, then we would need to explain why larger mammals were disproportionately affected. We would also need to explain why the extinctions were not synchronised across the globe. Why would climate change have wiped out Australian and European species before North American ones? And why did extinctions take place earlier in North America than in South America? We know that Homo sapiens colonised Europe and Australia before North America. We also know that our species entered North America from Eurasia – crossing the Bering Straits, which, thanks to lowered sea levels, were not under water during the Last Glacial Maximum (LGM) – and then took another thousand years to reach the southern tip of South America, which explains why extinctions came later on the more southerly continent. All this points an accusing finger at modern humans. Although our responsibility for the extinctions has been fiercely debated, the accumulated evidence is overwhelming. No doubt, the shifting climate played a role – perhaps a decisive one in some cases and a synergistic one in others – and we should not lose sight of that. Ecological processes, which would have driven these extinctions, are too complex to allow for simple explanations to dominate every extinction event. However, it is easy to envisage humans pushing megafauna over the edge, as it were, by hunting to extinction small and declining populations already stressed by climatic changes that were shrinking their habitats and reducing their food. There is one further point that we need to factor in: because of their great size, adults of these huge mammals had no natural predators, and thus had evolved no specific strategies against predation. As a result, when a new predator suddenly arrived on the scene, these naïve giants – naïve in the sense that they did not know how to deal with an enemy capable of killing them – would have made easy prey. And we humans were quick to take advantage of this. The archaeological record clearly shows that we hunted mammoths and other giant herbivores, eating the meat and working the skin into leather, and our relationships with these giant mammals are beautifully preserved in the Stone Age paintings of Lascaux in south-western France, and other such sites in 133

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Europe. Such realities should also perhaps prompt further consideration of the way in which traditional communities live ‘in balance with nature’. This is one of those myths modern society likes to perpetuate, possibly because it makes people feel better about themselves. We are all aware of the destructive and often exploitative nature of humans trapped in the ‘civilised’ lifestyle of cities and the commercial farmlands that feed them, and perhaps look to ‘indigenous peoples’ – whatever this term may mean – as a model of salvation for our own ecological sins.

MEGAFAUNA AND ECOSYSTEMS With the demise of megafauna around the globe, Africa is now the only continent on which the ecological processes driven by these giant mammals still continue to shape the landscape. But what exactly are these ecological processes – and what impact do they have? To investigate this question, let us return to Mauritius, that small granitic island 1 000 kilometres to the east of Madagascar that we visited in chapter 4. This might seem an odd place to start, as Mauritius never had megafauna in the conventional sense of the word – no mammals or land vertebrates weighing more than a ton. However, the island was home to two species of giant tortoises in the genus Cylindraspis, each weighing hundreds of kilograms, that were both hunted to extinction within two centuries of the arrival of the first human colonists. We might think of this as a shame, as we will never see these wonderful animals again.7 However, ‘a shame’ does not do justice to the importance of these giant reptiles to the ecology of Mauritius, La Réunion and Rodrigues. Recent research has shown that these tortoises were predominantly grazers – indeed, they were the only bulk grazers known on these islands – and we now suspect that they played an important role in dispersing the seeds of larger forest plants. To try to recreate the ecological services these tortoises provided, the Mauritian government introduced two related species to Round Island, an uninhabited islet off the north coast. These were the giant Aldabrachelys gigantea from the Aldabra Atoll in the Seychelles (figure 6.4) and the much smaller Astrochelys radiata from Madagascar, both of which belong to the Testudinidae – the family that also included the extinct genus Cylindraspis. Results so far have been encouraging. It appears that these non-native tortoises are grazing preferentially on 134

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Figure 6.4. A giant Aldabra tortoise (Aldabrachelys gigantea). Photograph by Ara Monadjem.

alien weeds and helping to disperse the seeds of at least one threatened native plant (Griffiths et al. 2010). We can piece together a similar story for other islands in the region. Madagascar, for example, had an abundant supply of super-sized species, including two endemic giant tortoises in the genus Aldabrachelys – the same genus that still survives in Aldabra Atoll today and has been introduced to several Mascarene islands. It appears that these tortoises were the primary dispersers of the seeds of all six of Madagascar’s baobab species (Andriantsaralaza et al. 2014). With these tortoises long gone, the baobabs have since struggled to disperse their seeds effectively. Archaeoindris was a gorillasized lemur. Members of the genera Megaladapis and Palaeopropithecus were smaller, but at about 50 kilograms they were still giants compared with today’s lemurs (Goodman and Jungers 2014). Megaladapis, also known as the koala lemur, had a squat body with long arms and feet, adaptations for an arboreal existence. Palaeopropithecus, or the sloth lemur, was also arboreal but probably moved through the vegetation by swinging from branch to branch, perhaps in the same manner as sloths of South America today. The island was also home to at least three species of hippopotamus, one almost as large as the common 135

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hippopotamus of Africa (Hippopotamus amphibius) and two dwarfs. All these species are now extinct, and most of them were fed on by humans once they colonised Madagascar in the past two or three millennia (Perez et al. 2005).8 In fact, all lemurs larger than 10 kilograms – and there were at least 17 species of them – are now extinct (Crowley 2010); in each case extinction followed the arrival of humans on the island. Madagascar was also home to up to 11 species of elephant bird (family Aepyornithidae). These flightless, feathered giants belonged to the ratites – the same group that includes today’s ostriches, emus, cassowaries, rheas and kiwis. They included the largest birds that ever lived, some reaching a weight of up to 500 kilograms, and were therefore the second-largest terrestrial animal in Madagascar in recent times after the now extinct hippopotamuses. Most died out more than a thousand years ago, with some hanging on for a few hundred years more but ultimately going the same way. We would therefore expect them to have played an important role in structuring the Malagasy ecosystem – and that does, indeed, seem to be the case, judging by the structure of many plants in the region (Bond and Silander 2007). These plants have a divaricate, or ‘zigzag’, branching pattern. If you pull a divaricate branch from its end – in the manner of an ostrich plucking at a blade of grass – you can stretch it out some distance. When you release it, however, the branch springs back to its original zigzag shape without breaking. I once tried this ‘trick’ at the invitation of William Bond, with whom I was teaching on a Tropical Biology Association field course at Kirindy in Madagascar. He pointed out how the same divaricate branching pattern is exhibited by plants in New Zealand, which was once home to the moas (order Dinornithiformes), another extinct island group of large, flightless birds. It appears that this interesting plant morphology is shared by the remote and unconnected islands of Madagascar and New Zealand because they shared a similar browsing guild of large birds – as opposed to large mammals that, thanks to their teeth, would have had no problem dealing with such divaricate branches.

THREE CRITICAL ECOSYSTEM ROLES PLAYED BY MEGAFAUNA Our studies of African landscapes suggest that megafauna play three critical roles in ecosystems (Malhi et al. 2016). First, giant mammals such as elephants, rhinoceroses and hippopotamuses dramatically change the structure and composition of 136

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the vegetation. Second, these changes have a cascading effect down though the trophic levels, affecting a large number of animals.9 Third, megafauna help to recycle nutrients that are often bound up in an otherwise unusable form, such as old branches, making these nutrients available to a host of other species and thus enriching entire ecosystems. Let us now look at these three roles in greater detail. Changing the structure and composition of the vegetation If you have watched an elephant in an African savanna, you might have observed it feeding. Usually this involves nothing much more exciting than the elephant tugging at a branch or large tussock of grass, which it then unhurriedly bundles into its mouth and chews endlessly. However, you may occasionally be rewarded with something a bit more riveting, such as watching it uproot a small shrub and proceed to eat the entire plant – even its roots. Very occasionally you might even be entertained by the sight of a large bull elephant pushing down a big tree with his forehead (figure 6.5). At this scale, the impact on vegetation structure is obvious. As elephants uproot shrubs and push down trees, they open up woodlands and turn them into grasslands. This basic mechanism

Figure 6.5. An acacia tree recently pushed over by elephants in Serengeti National Park, Tanzania. Photograph by Mike Unwin.

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has driven ecological processes in terrestrial ecosystems across the globe. Yet, because the collective memory of humanity extends dozens of millennia short of the true ‘Age of Mammals’, we rejoice in our forests and view any agent of their destruction as something negative. We have lost sight of the fact that megafauna have been selectively ‘destroying’ forests for millions of years. In fact, thanks to the tireless efforts of these animals, landscapes dominated by megafauna experience greater levels of heterogeneity than those from which they are absent, allowing room for more species to pack into the same area. This may at first seem contradictory, but on reflection it makes sense. A continuous, unbroken woodland will be home to a variety of mammals and other organisms that have the skills to forage for food, find roosting and denning sites, and avoid predators in that particular environment. But it will not be home to species with other skill sets that allow them to, say, exploit a grassland. A woodland antelope such as a duiker tends to act furtively in the presence of a predator, preferring to slink away unobtrusively rather than flee at top speed. Natural selection has thus favoured individuals that were appropriately camouflaged. Such skills are of less use in an open savanna, where a predator may see the antelope from hundreds of metres away; in such open environments, fleet-footed antelopes, such as gazelles, will prevail.10 As a result, woodlands and open grasslands typically have very different assemblages of antelope. From this, we would predict that a landscape with a patchwork mosaic of both woodland and grassland will support the greatest number of antelope species. And this is exactly what we find in nature. Cycling nutrients within an ecosystem Megafauna also play a vital ecological role by encouraging the continual cycling of nutrients within an ecosystem. In a woodland ecosystem, many nutrients are locked up in the woody stems of the shrubs and trees that constitute it. Such woody matter is practically indigestible to the majority of animals, effectively locking these nutrients out of circulation. The obvious result of reduced nutrient flow through an ecosystem is its impoverishment. Megafauna, however, are able to break down and digest woody stems, thereby speeding up the process of decomposition, which eventually releases the locked-up nutrients back into the ecosystem. Instead of perceiving an elephant as the destroyer of trees, then, we should perhaps view it as the liberator of energy that would

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otherwise not be available to boundless other organisms. Megafauna also spread abundant nutrients in the form of their faeces, effectively fertilising the landscape. It has recently been calculated, for example, that hippopotamuses introduce 3 125 tons of dry plant matter to the Mara River in east Africa each year, of which 1 277 tons is carbon, 180 tons is nitrogen and 18 tons is phosphorus (Subalusky et al. 2015). Without such glorious amounts of ordure entering the system via the digestive tracts of hippopotamuses, which graze on the plains at night, the river would undoubtedly be unable to maintain its high densities of fish – not to mention the crocodiles, fish eagles and many other creatures that feed on them (figure 6.6). And that is not the end of the story with hippos. These huge animals act as hydrological engineers, both by creating deep pools through their regular wallowing in mud (Naiman and Rogers 1997) and by clearing and maintaining waterways as they bulldoze their way through wetlands such as Botswana’s Okavango Delta (McCarthy et al. 1998),

Figure 6.6. A channel in the Okavango Delta, bustling with life, thanks to the ecosystem services provided by the hippopotamus (Hippopotamus amphibius). Photograph by Ara Monadjem.

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on their regular foraging trails. These hippo-created channels and water bodies are vital for nutrient flow through the system, and also act as corridors for fish, allowing them to reach otherwise isolated pools. They may even reshape the geomorphology of the wetland by focusing erosion and incising new channels that alter the direction of water flow. The ecological role of hippopotamuses in aquatic habitats thus neatly complements that of elephants in savanna and woodland ones. Is the presence of megafauna always beneficial? You may have perceived a slight problem with this theory. If megafauna bring such benefits to the landscape, by creating heterogeneity and increasing biodiversity, why is it that in some circumstances they seem to be doing exactly the opposite? You might cite the current situation in South Africa’s Kruger National Park, for example, where the doubling of elephant numbers over the past two decades, leading to visible changes in the landscape, has seen a concomitant decline in certain other species. Eland (Tragelaphus oryx), roan antelope (Hippotragus equinus) and tsessebe (Damaliscus lunatus) have all but vanished from the southern half of the park. Could it be that elephants have ‘destroyed’ the habitat that these three species require? In fact, it would appear that elephants have had little or nothing to do with their decline. Predation by lions has been the dominant factor, mediated through the many humanmade waterholes scattered around the park. These waterholes – which are an artificial addition to the landscape – attract large numbers of ungulates during the dry season, bringing with them lions and other large predators. Thanks to the permanent availability of water, and thus prey, lion densities remain high throughout the year and throughout the park. Before the waterholes were constructed, large areas of the park were unavailable during the dry season to water-dependent antelope such as buffalo that need to drink regularly. This regulated the density of the lion population, with zones of high lion abundance, typically along perennial rivers, and zones of low lion abundance, largely in zones where many of these waterholes are now situated. I have taken this little detour to make an important point about ecology and science in general: it is easy to attribute an observed correlation to the wrong cause. In this case, the antelope decline in the Kruger National Park had nothing to do with elephants; it was driven by predators. 140

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Nonetheless, we have to be careful when claiming that because megafauna have occurred on Earth for hundreds of millions of years, their presence is always desirable in any ecosystem that once supported them. This is because of another important consideration in ecology: that of scale. At the scale of a shrub or tree, say, the uprooting of a plant by an elephant will be highly destructive because that plant is not immediately replaced. However, at the slightly larger scale of a ‘patch’ – such as an area the size of a soccer pitch – the removal of the tree represents an opening in the woodland, which helps to create a new and productive habitat. In other words, exactly the same action – an elephant removing a tree – has different repercussions at different scales. Megafauna, without a doubt, have been present for a very long time, and they have shaped ecosystems and provided numerous beneficial ecological services. However, at no time before the present have megafauna been restricted to relatively small geographic areas by artificial barriers. In effect, this is what we have done by creating parks and placing fences, or farms and angry farmers, around them, restricting elephants and rhinoceroses mostly to our larger parks and reserves. Such confinement alters impacts at different scales. In the days before fences, when African megaherbivores roamed freely, it was unlikely that their populations would build to unsustainable numbers in any one location, because they were able to move out of stricken areas – perhaps not returning for decades or even centuries. Such long-term natural cycles played out on vast spatial scales, covering areas the size of countries and possibly even continents.

THE ELEPHANT PARADOX As I said earlier in this chapter, today elephants are the largest of the world’s megafauna. Their role in Africa’s ecosystems warrants special consideration, especially given the changes that humans have now brought to their landscape and the relative confinement into which they have consequently been forced. Let’s remind ourselves of the ‘elephant paradox’ that I mentioned in chapter 1. As we have seen, megafauna play a critical role in savanna ecosystems, allowing more species to coexist in a particular area. The savanna elephant has declined dramatically in distributional range and numbers, and will become extinct unless we conserve the species in parks and other protected areas. However, where elephants have been successfully protected and their numbers have built up, 141

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they have denuded the savanna, removing every last tree and shrub, destroying nesting and roosting sites and leading to measured losses in biodiversity. In the Kruger National Park, for example, elephants have effectively sterilised the abundant and widely distributed African palm (Hyphaene petersiana), because their relentless foraging and cropping has prevented it from reaching sexual maturity (Midgley et al. 2020). In summary, both the complete extirpation and the successful conservation of elephants are having equally damaging effects on their habitat. It is embarrassing to admit that, despite at least half a century of dedicated research on elephants, we ecologists still do not really have a solution to this dilemma. This has much to do with the politicisation of ecology as it pertains to elephants. The adoption of these charismatic giants as icons of African wildlife has polarised conservationists into two camps: those who wish to manage elephants for, say, trophy hunting and the selling of ivory, and use these profits to advance general conservation objectives; and those who feel that absolutely no management of elephants is either needed or wanted. This debate, which is more about the politics of conservation than conservation itself, has significantly hindered scientific investigations into important questions regarding the ecological role of elephants. It doesn’t help matters that, when it comes to the science of elephant conservation, egos are typically quite large – to the extent that some researchers in this field claim to know all the answers already. In such a volatile academic environment, it can be rather difficult to garner support for new research. However, this malaise has not affected all ecologists, and some interesting work is just starting to emerge from several quarters. One of the teams addressing the ‘elephant problem’ is that of the American ecologist Bob McCleery and the South African researcher Laurence Kruger, who are working in South Africa’s Kruger National Park and neighbouring Eswatini. I have had the good fortune to be able to work alongside these two brilliant field ecologists, and will try briefly to synthesise the findings of their several years of carefully crafted field studies. McCleery is a very likeable American, currently a professor at the University of Florida, while Kruger is an equally likeable South African, attached to the University of Cape Town but based at Skukuza, the ‘capital’ of the Kruger Park. McCleery comes out twice a year to Africa to conduct his fieldwork; once in ‘summer’ (the austral winter) with a group of University of Florida students on a study-abroad trip to learn hands-on ecology, and once in the austral summer on a shorter research trip. His base 142

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is the Savanna Research Centre at Mbuluzi Game Reserve, in north-eastern Eswatini. This is where I usually join him, with a few students from University of Eswatini (figure 6.7). This study-abroad course is as much about learning how to interact with people from different social and cultural backgrounds as it is about developing field skills. Over the last few years, on McCleery and Kruger’s courses, we have been assessing the presence and relative densities of a wide variety of terrestrial vertebrates, including terrestrial small mammals, mesocarnivores, ungulates, bats and birds. Simultaneously, we collect data on the structure of the vegetation, noting, for example, the amount of ground covered by various layers of vegetation – from grasses to the canopies of the largest trees. This is demanding work. The team rises well before sunrise so that the birders can be out recording birds at dawn

Figure 6.7. American and Emaswati students collecting ecological data in Hlane Royal National Park, Eswatini. Seated on the left is Charles Gumbi, who was completing a PhD at the University of Florida at the time this photograph was taken, after doing his undergraduate and MSc degrees at the University of Eswatini. Photograph by Ara Monadjem.

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when avian activity peaks. Shortly after the birders’ departure, the small mammal crew gets going; we have to check the metal Sherman live traps early to ensure that they have been emptied of small mammals, which are released unharmed, before the African sun bakes them alive. Later still, the teams responsible for the camera trap (set for medium-sized and large mammals) and bat detector (to record bat calls from which we can deduce which species were flying around) head out to do their stuff.11 All of these surveys have been carefully planned by McCleery to ensure that we collect all the necessary detail needed for future analyses. At around mid-morning the various teams gather together to do ‘veg’ (collecting information on vegetation such as grass biomass or shrub cover). I have to admit that, as a zoologist, I find doing ‘veg’ a trifle challenging. For a start, there is no real excitement. There is nothing to catch, as plants do not run away from you, and no traps to check to see what creature you have captured – a process that never ceases to thrill zoologists. ‘Botanising’ in the field with a botanist (figure 6.8) – that is, examining and identifying every species of plant – can still be enjoyable for a zoologist, especially since it’s the only way that most of us learn any new plant names! But doing ‘veg’ is mindnumbing work that, for example, requires one to walk hundreds of metres in a straight line through thorny acacia thickets holding a 5-metre-long pole and shouting out a measurement every few steps. At the end of the day, however, these measurements are critical for quantifying the habitat of the animals we are studying, so we support Kruger in his endeavours, mostly by leaving him alone to get his work done. These plant and animal surveys have been conducted in identical ways and across two seasons in both the Kruger National Park and Eswatini (figure 6.9). The habitat in both locations is similar, consisting of savanna dominated by similar species of grasses, shrubs and trees such as marulas (Sclerocaryea birrea) and knob-thorns (Senegalia nigrescens). However, there is one crucial difference: in Kruger, megafauna are present; in Eswatini they are absent. We have been amazed by the results. No matter what criteria you go by, the Eswatini sites are ‘doing better’. They show a greater variety of vegetation structure, greater heterogeneity and a higher number of species living at higher densities (McCleery et al. 2018). In other words, the sites with megafauna are not more diverse, as we might have predicted following what we learned earlier in this chapter. Not only is diversity lower in Kruger; it is much lower. On average, the Eswatini sites have double the diversity of the Kruger sites. You might wonder whether the 144

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Figure 6.8. Laurence Kruger demonstrating how one should be doing vegetation analyses: on one’s hands and knees with one’s face close to the ground. Note the fence in the background, a herbivore exclosure camp in Gorongosa National Park, Mozambique, where similar processes are being studied to those described in this book taking place in the Kruger National Park and Eswatini. Photograph by Tara Massad.

smaller numbers of species that find Kruger an agreeable environment in which to occupy themselves with life’s tasks include any rare or threatened species. If this were the case, then we would happily accept the loss of a few – or even many – common species. But it is not. What’s more, when we plotted the ecosystem services being provided by our study animals in Eswatini against those in Kruger, again the Kruger ecosystem came up far short. In every possible sense, the Kruger sites are impoverished. How do we account for this disparity? Do we blame elephants, rhinos and hippos? It is tempting to do so; the correlations are so strong. However, as we have seen, correlation does not imply causation. To be able to disentangle the impact of elephants from other possible agents, we need to conduct a series of experiments – elephant manipulation experiments, to be precise. This can 145

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Figure 6.9. Bob McCleery inspecting an Anabat bat detector in the Kruger National Park with an elephant (Loxodonta africana) in the background. Several of our camera traps have been destroyed by elephants. Photograph by Ara Monadjem.

be done by, for example, fencing off small areas within the Kruger National Park and measuring the responses of the vegetation and the various animals we have been studying. We need to be careful how we set up our fences, though. If we exclude all large mammals – say, from duiker-size upwards – then we could not be sure whether the causal agent was elephants or some other species, or group of species. Fortunately, it is possible to fence off only elephants, and allow smaller species through under the fence. Exactly such an experiment has recently been set up in the Kruger Park – the fences were completed in 2019 – and has been replicated in Eswatini in 2022. We hope to have some preliminary results within a year or two, but in the meantime, all that we can do is wait patiently. Ideally, we would want to do a reverse experiment in Eswatini by introducing elephants into areas where they have been absent for more than a century. In fact, such an ‘experiment’ has already been conducted at Hlane Royal National Park, a relatively large – by 146

Plate 1. A collage of African bats. From top left, clockwise: Hypsignatus monstrosus; Rhinolophus hillorum; Macronycteris vittatus; Taphozous mauritianus; Mops leonis; Nycteris arge; Miniopterus nimbae; Scotophilus nux. Photographs by Ara Monadjem.

Plate 2. A brush-furred rat (Lophuromys sikapusi ), a beautiful and abundant rodent of the Upper Guinea rainforest zone of west Africa. Photograph by Ara Monadjem.

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Plate 3. An arboreal tree rat (Thallomys paedulcus) climbing a bush at Satara Rest Camp in the Kruger National Park, South Africa – note the long tail that is used for balance. Photograph by Mike Unwin.

Plate 4. A bush squirrel (Paraxerus cepapi ) in the Kruger National Park, South Africa. This is a common sciurid in the savannas of southern Africa. Photograph by Ara Monadjem.

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Plate 5. A tiny 8-gram shrew (Myosorex meesteri ) captured in the Chimanimani Mountains, Mozambique. Photograph by Ara Monadjem.

Plate 6. The highly localised and threatened Nimba otter-shrew (Micropotamogale lamottei), photographed beside a small stream in the East Nimba Nature Reserve, Liberia. Photograph by Ara Monadjem.

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Plate 7. A yellow-spotted rock hyrax (Heterohyrax brucei ) in Hwange National Park, Zimbabwe. Photograph by Mike Unwin.

Plate 8. A dwarf mongoose (Helogale parvula) stretching on a fallen tree trunk in the Kruger National Park. Photograph by Ara Monadjem.

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Plate 9. A herd of savanna elephants (Loxodonta africana) in Tsavo National Park, Kenya. Note the barren landscape, created by the activities of the elephants themselves. Photograph by Ara Monadjem.

Plate 10. A small herd of wildebeest (Connochaetus taurinus) in the Kruger National Park, with a calf standing next to its protective mother. Photograph by Ara Monadjem.

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Plate 11. The largest herd of zebra (Equus burchelli ) and wildebeest (Connochaetes taurinus) I have ever seen, in the Maasai Mara National Reserve, Kenya, in 2009. The distant black and white dots are all individuals of these species; wherever I looked I saw more such dots. Photograph by Ara Monadjem.

Plate 12. Zebra (Equus burchelli ) and wildebeest (Connochaetes taurinus) in Ngorongoro Crater, Ngorongoro Conservation Area, Tanzania. Photograph by Mike Unwin.

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Plate 13. A white rhinoceros (Ceratotherium simum) with its horn removed by game rangers in the Kruger National Park, in order to stem the tide of poaching. From 2013 to 2017, more than 1 000 rhinoceroses were illegally killed annually in South Africa alone, resulting in severe population declines for both rhinoceros species (Ferreira et al. 2021; Nhleko et al. 2021). Photograph by Ara Monadjem.

Plate 14. Common chimpanzees (Pan troglodytes) in Kibale National Park, Uganda. Photograph by Mike Unwin.

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Plate 15. A cheetah (Acinonyx jubatus) in the Central Kalahari Game Reserve, Botswana. Photograph by Mike Unwin.

Plate 16. A spotted hyena (Crocuta crocuta) waiting patiently, if somewhat frustrated, below a tree in which a leopard is feeding on an impala carcass. The blood covering the hyena’s head has dripped down from the carcass above. Photograph by Ara Monadjem.

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Eswatini standards – protected area in the north-east of the country, adjacent to Mbuluzi. Elephants were reintroduced to Hlane in the 1980s, where they were confined to two ‘camps’, each about 1 000 hectares in extent. This was necessitated, at the time, by the lack of funds to fence the entire park, and the elephants have remained in these two enclosed areas ever since. Monitoring the state of biodiversity within them would give us a different angle on the same research question. We will return to the ‘elephant paradox’ in chapter 10. For now, however, I should note that even though we have undeniably demonstrated a significantly lower species richness and ecosystem functioning – associated with a more homogenous vegetation structure – at our Kruger sites, this does not mean that things are all bad in Kruger. We are not making value judgements – saying, for example, that Kruger has been ‘trashed’, ‘destroyed’, or otherwise altered in some negative way. We are simply reporting what we have found. This may come as a surprise, although it should not. Science cannot tell us whether Kruger is in a better or worse shape than it was, say, two decades ago. There is no law in ecology that says a more diverse ecosystem is necessarily a better ecosystem. We can show that diverse ecosystems are, for example, more resilient to alteration – by ­climate change, for example, or invasive alien species. Or we can prove that diverse ecosystems provide more ecological services, such as plant pollination. However, when it comes to choosing whether we would prefer a diverse ecosystem providing many ecological services or an impoverished one offering few services, we must first ask ourselves what we humans want from that system. *** In this chapter, we have looked at how large mammals are instrumental in shaping ecosystems by affecting the structure of vegetation, habitat heterogeneity, trophic relationships and nutrient cycling. We have focused on the largest of these mammals, the megafauna (species weighing upwards of one ton), since these make the greatest impact on the landscape. We have seen how megafauna roamed the Earth for hundreds of millions of years and in a prolific variety of forms, but were quickly removed following the arrival of a new super-predator, Homo sapiens. As megafauna disappeared, so humans scrambled to occupy all available habitats, leaving a trail of destruction across the globe. The one exception to this pattern was in Africa, where slightly less than half the megafaunal component managed to hang on – presumably because African wildlife had 147

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evolved alongside humans and had thus developed adaptations to avoid being captured or killed. Today, megafauna are gone from much of the planet, being absent from the Americas, Australia and more recently Eurasia. A single species of elephant and one genus of rhinoceros survive in South and South East Asia, but from an ecological perspective megafauna are all but gone from that region too. For us to understand the ecological role of megafauna, therefore, we are left with just one continent on which to conduct our studies: Africa. And having identified how that continent’s ecosystems have been shaped, we can now investigate more closely how so many different species manage to coexist within them. This is what we will do in the next chapter.

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S

o far in this book, we have examined the forces that have shaped African fauna over big expanses of both time and space. In this chapter we will zoom in closer and observe on a finer scale how species distribute themselves in the here and now. This is the domain of ‘community ecology’, which seeks to understand how species arrange themselves into groups that give the appearance of organised communities.

INDIVIDUALS OR SUPER-ORGANISMS? At the core of community ecology lies a centuries-old debate: do species react individually to changes in the environment, or do they instead assemble into organised communities? We need to understand this difference, because it lies at the heart of the debate. The great German naturalist and explorer Alexander von Humboldt (1769–1859) developed, almost from scratch, the field of plant geography. He surmised that different plant species are bound together in vegetation associations that can be defined by their life forms – namely, their general appearance and habits. He based his conclusions on his Andean expedition of 1801–1803, during which he meticulously recorded the species of plants occurring at various forest sites up steep elevational gradients (Wulf 2015). This may not sound novel today, in an era when the concept of vegetation types is

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widely understood, but it was a far cry from the practice of the times, which dictated a focus on individual species rather than on plant communities. A century later, this concept was further developed by Frederic Clements who, in 1916, likened plant communities to ‘super-organisms’ and contended that each community functions as an organic entity (Nicolson 2013). In other words, when we look at a savanna or forest, we are not observing a collection of different species eking out their livings individually at the same location, but rather seeing a highly interconnected and integrated system that has collectively, so to speak, a life of its own. Furthermore, this super-organism has emergent properties.1 This became the informed position of botanists for several decades, with Henry Gleason representing a lone voice to the contrary. Gleason argued that plants respond individualistically to environmental changes (such as gradients in elevation or temperature) and to biotic interactions such as predation and competition. Therefore, the ‘community’ that we see is simply a snapshot of a particular landscape at a particular point in time and, when viewed over an extended period, turns out to be an illusion. In Gleason’s view, individual species are continually added or removed from a ‘community’ over time, as changing conditions encourage or discourage them. The extreme version of the super-organism view of life is the Gaia hypothesis proposed by James Lovelock and Lynn Margules in the mid-1970s (Lovelock and Margules 1974). I will not go into the details of this theory here because it is only tangentially relevant to our story, but because of its influential history it might be of passing interest. At the root of the Gaia hypothesis is the idea that the Earth is a finely tuned, self-regulating system that ensures that environmental conditions remain suitable for life. In other words, Earth itself is the ultimate super-organism, with an internal ‘thermostat’ that keeps life ticking over. This hypothesis caused much debate and interest in the 1980s and early 1990s, but unfortunately – for it is a beautiful concept – this is not how our planet functions. It is true that environmental and biotic components influence one another with feedback loops that may regulate certain processes. However, there is no ‘thermostat’, and we now know that the Earth’s climate has been anything but stable, as I discussed in chapter 5 (Simberloff 2014; Tyrell 2013). Simply put, the idea of the ‘balance of nature’ is a myth. Zoologists have also been preoccupied with this concept of ‘community’. At the same time that Clements and Gleason were debating the nature of plant communities, Joseph Grinnell and (a decade later) Charles Elton were developing 150

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the concept of the niche, which would be fundamental to our understanding of how animal assemblages are structured (Soberón 2007). After a century of refinement, the ideas of these two ecologists have been labelled the ‘Grinnellian’ and ‘Eltonian’ niches, respectively, and it is worth examining them here, since we will refer to them again later in this chapter. Understanding niches The word ‘niche’ has been used widely and loosely by ecologists, and therefore has the potential to confuse – especially in relation to the closely related term ‘habitat’. In an attempt to bring some rigour to the way we use these two terms, the ecologists Robert Whittaker, Simon Levin and Richard Root defined ‘habitat’ as the physical set of characteristics that define the area in which an animal lives, and ‘niche’ as the functional role, or ‘way of life’, of a species (Whittaker et al. 1973). For example, the habitat of an animal may be ‘rocky outcrops in savanna’, whereas its niche may be ‘small, diurnal, crevice-dwelling insectivore’. Hence, two species may appear to be occupying the same habitat (such as savanna) but have different niches within it. The white and black rhinoceros (Ceratotherium simum and Diceros bicornis, respectively) can be seen side-by-side sharing the same savanna habitats in parks across South Africa. Within each park, however, the black rhinoceros selects closed woodlands and thickets while the white rhinoceros typically prefers open grasslands, which represent differences in habitat choice. This in turn reflects their completely different diets: the black rhinoceros browses on the leaves and twigs of woody plants, while the white rhinoceros grazes on grass, which represents differences in their niches. The one person who has probably had the greatest influence on developing the concept of the niche is Evelyn Hutchinson (1903–1991), who lectured at the University of the Witwatersrand in the 1920s and is regarded by some as the father of modern ecology (Slack 2011). Hutchinson defined a niche as a mathematical abstraction: a hypervolume with multiple axes, each one representing a different physical feature or resource that a species requires in order to persist at that location.2 He further distinguished between the ‘fundamental niche’ and the ‘realised niche’. The former describes the niche of a species in an idealised world without predators and/or competitors; the latter describes the actual niche in the presence of all biotic elements. However, Hutchinson may have 151

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unintentionally introduced a large dose of confusion by representing the niche as a property of the species, as opposed to a ‘place’ or ‘situation’ in nature. It appears that ecologists have finally reached a consensus on the definition of a niche that has been divided into a Grinnellian component and an Eltonian one, as follows. The Grinnellian niche focuses on environment variables that relate to the broad-scale ecological and geographic properties of species. This has been likened to the performance of the species in the context of its environment (Devictor et al. 2010). The Eltonian niche, in contrast, emphasises biotic interactions (such as predation and/or competition) and resource dynamics (such as food), which can be measured at local scales (Soberón 2007). This has been likened to the impact that a species has on its environment and, as a result, is frequently associated with its morphology – for example, the teeth of a mammal, which, to a large extent, determine its choice of food. Furthermore, both these niche concepts can be viewed as either fundamental or realised, as developed earlier by Hutchinson.

BATS AND COMMUNITY STRUCTURE We are now ready to consider what community ecology means in African mammal communities. One person who has set out to answer such questions is my colleague Corrie Schoeman, formerly of the University of KwaZulu-Natal, South Africa. His depth of reading and curiosity in things well beyond his academic field makes for conversation that is always interesting and usually highly educational. One question that has long preoccupied him is this: what factors act to filter out species, from the pool of all possible species occurring in the region, at a particular locality? Let us imagine, for example, that 40 species of bat are known to occur in a particular region that covers an area of 1 000 square kilometres, but when we focus on one particular site of a few hectares within this region we record only 22 species. Why are the other 18 species not present there? Does it have to do with the absence of suitable habitat? This is unlikely, as we carefully chose the locality we are studying to reflect the conditions that are present across the broader region. Perhaps it has to do with competitive interactions between similarly adapted bats that use the same environment in a similar way – for example, by feeding on similar food types. The so-called ‘­competitive exclusion principle’ dictates that if two species have identical diets, 152

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and their foods are available in limited quantities, then one will predominate and the other will disappear.3 Alternatively, perhaps the filter is not related to competition but to predation. For example, a species has been wiped out by a predator, or the mere presence of a predator has created a ‘landscape of fear’ that causes certain species to avoid that specific locality. Perhaps disease has also played a part. Disentangling these various explanations is not an easy task; it requires carefully designed fieldwork and the clever application of appropriate statistical tools. Thankfully, these are activities in which Schoeman excels. In partnership with David Jacobs, a distinguished evolutionary biologist from the University of Cape Town, he set out to answer the question of what was structuring bat communities in South Africa (Schoeman and Jacobs 2011). To this end, he conducted extensive surveys at six localities covering four of the six biomes present in the country: fynbos, Nama karoo, savanna and forest. Each bat that was captured was carefully examined and its wing area measured. The shape of a bat’s (or bird’s) wing, like that of an aircraft’s wing, tells us about its flying abilities (figure 7.1).4 For example, broad, rounded wings such as those of a horseshoe bat (family Rhinolophidae) are useful for flying slowly

Fruit bat

Clutter

Open-air

Edge

Figure 7.1. Differences in the shape of the wings of bats. Clockwise from top left: the broad and large wings of fruit bats that need to cover long distances to find fruiting trees; shorter and rounder wings needed to manoeuvre through tangled vegetation; the intermediate wing shape useful for exploiting edge habitats; long, narrow wings allowing fast flight in open situations.

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through a dense forest, providing manoeuvrability. In contrast, long, narrow, pointed wings such as those of a free-tailed bat (family Molossidae) allow for fast flight in open environments – for example, above the forest canopy. In fact, insectivorous bats can be categorised into three main groups based on their wing morphology: ‘open-air’ species that fly fast and above the canopy; ‘clutter’ species that fly slowly in dense vegetation such as forest; and ‘edge’ species that fly at intermediate speeds on the boundary of open and forested situations (Schnitzler and Kalko 2001). Schoeman also recorded the echolocation calls of each bat using a specialised bat detector. Different types of bat detector function in different ways, but the important point is that they allow us to record the ultrasonic calls of bats and view them on a computer screen at our leisure. Like relative wing shape, the echolocation call of a bat reflects the sort of environment that it can fly in. Typically, low-frequency calls (low in comparison to other bat calls, though still far too high-pitched for humans to hear) carry further than high-frequency calls, which attenuate rapidly. Hence, bats flying in open environments, such as fast-flying free-tailed bats, have lower-pitched calls than those, such as horseshoe bats, flying in dense, cluttered environments. This is, of course, an oversimplification, but the important point is that we can match the calls of bats to specific habitats. Finally, Schoeman also collected faeces from each bat for later microscopic analysis of its diet. This is tedious work that – as I can testify – can only be accomplished through serious determination or excessive enthusiasm. The insect species extracted from the faeces were then compared with those that occurred in each locality, captured by Schoeman in insect traps, to see whether the bats were selecting certain species or simply taking insects according to their abundance. In essence, what Jacobs and Schoeman were testing was whether the niches of South African bats, specifically the Eltonian niches, had been shaped by competition, predation, or some other factor. After several years of dedicated field and laboratory work, they were able to show that bat communities in South Africa had not been structured by inter-species competition. If competition had been a factor, we would have expected the diets of different species to differ because competition would have ‘forced’ them apart over evolutionary time. Instead, the study found significant overlap in the diets of different species. Furthermore, they found that the best predictor of a bat’s diet was the frequency 154

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(pitch) of its echolocation call (figure 7.2): those bats with high calls consumed a greater proportion of moths. The reason for this is in fact an interesting story in itself. Some moths have ‘ears’ – not large flaps of skin and cartilage as in a typical mammal, but a sound-sensitive tympanum located on the thorax that is able to detect airborne vibrations and hence bat echolocation calls – which have evolved in an arms race with the bats that are targeting them.5 The ears of each moth species are typically tuned to a particular frequency band that is determined by the echolocation call of the bat species that feeds on it (Zha et al. 2009). To counter this, the frequencies of bat calls have increased in order to ‘reach over’ the sensitive frequency range of the moths, enabling them to capture these moths undetected. This arms race between eared moths and bats is an example of coevolution. This is a common phenomenon in nature that often involves predators and prey but can also be seen in parasite–host interactions. We modern humans, with our chemical defences, may have forgotten what it feels like to be overrun by 110 100 90 80 70 60 50 40 30 20 10 0 4.938 s : 32.6 kHz

Soothing: Auto

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Figure 7.2. A spectrogram (or sonograph) depicting the echolocation call of a bat in graphical form that was recorded near Manzini in Eswatini. Some 11 notes (pulses) can be seen, each a separate call from the same individual. The horizontal axis shows time (each note is separated by milliseconds). The vertical axis shows frequency (or pitch) and it can be seen that each note begins at a higher ­frequency that drops off to a lower one over time. The frequency, length and shape of such echolocation notes can frequently be used to identify the unseen (free-flying) bat, but in this case could refer to one of several species with similar calls.

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parasites – both the externally visible ones, such as lice, ticks and fleas, and the internal ones, such as tapeworms. However, the life of a typical organism involves a daily battle against parasites, and it is a battle that can never be won. Our understanding of this reality was dubbed the ‘Red Queen Hypothesis’ in the 1970s, invoking a line from Lewis Carroll’s Through the Looking Glass, in which the Red Queen says to Alice: ‘Now, here, you see, it takes all the running you can do, to keep in the same place’ (Van Valen 1973). Unlike competitive interactions, predatory ones (including parasitism) take place over different trophic levels and therefore the evolutionary pressure is constant. Competition only becomes an issue if a particular resource, such as food or a nest site, is limiting. But for possibly long periods of time when population levels are low (see chapter 8), competition may be weak or nonexistent. This is not the case for interactions across trophic levels, because organisms always need to feed. One example of interaction across trophic levels is predator–prey coevolution. African savannas are world-famous for their large herds of plains antelope, which are prey for up to five large predators: lion (Panthera leo, figure 7.3), leopard (Panthera pardus), cheetah (Acinonyx

Figure 7.3. A lion (Panthera leo) feeding on an elephant carcass in Hwange National Park, Zimbabwe. Photograph by Mike Unwin.

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jubatus), spotted hyena (Crocuta crocuta) and African wild dog (Lycaon pictus), also known as African painted wolf. In South Africa’s Kruger National Park, the competitive interactions between these large carnivores and the 22 ungulate species on which they prey have been documented by Norman ­Owen-Smith and Gus Mills (Owen-Smith and Mills 2008). Based on the analysis of a unique dataset of almost 50 000 ungulate carcass observations created from reports made by the park’s field staff over a 46-year period, they showed that the 5 predators had distinct dietary preferences, presumably thereby reducing competition between them. However, the interaction between the predators and their prey brings coevolution into play: for the predators to survive, they must capture and consume their prey; for the prey to survive, they must prevent precisely this from taking place! As prey have evolved to become larger and more fleet-footed, so predators have done the same. A recent study by Yonghua Wu and colleagues examines the diel – or daytime/night-time – activity of ungulates and carnivores (Wu et al. 2018). Today, most ungulates are diurnal, conducting most of their activities during the day. In contrast, most mammalian carnivores are nocturnal. However, by examining the genes involved in the development of rods and cones in the eye, this study was able to show that the ancestral carnivore was diurnal whereas the ancestral ungulate was nocturnal.6 Carnivores, then, shifted their activities from diurnal to nocturnal in order to tap into the ungulate food source. Based on this evidence, the authors of the study speculated that ungulates subsequently shifted their diel activity from a predominantly nocturnal one to a diurnal one in order to avoid carnivores. Let us now return to bats. In an appealing piece of research, Corrie Schoeman, Steve Goodman and their colleagues examined the radiation of the long-fingered bats (genus Miniopterus) in Madagascar (Schoeman et al. 2015). As we saw earlier, there are at least 12 species of the genus Miniopterus endemic to Madagascar. By comparison, mainland Africa – which represents a surface area 50 times greater than that of Madagascar – has exactly the same number of species (figure 7.4) (Monadjem et al. 2019; Monadjem, Guyton et al. 2020).7 Specifically, Schoeman, Goodman and their team of researchers were testing two competing hypotheses for how this radiation occurred, which bring into sharp contrast the concepts of the Grinnellian and the Eltonian niche we explored at the beginning of this chapter. One hypothesis, the ‘Habitat First Rule’, suggests that an ancestral species colonising a new area rapidly diversifies into new species to occupy different available habitats prior to dietary 157

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Figure 7.4. A Villiers’ long-fingered bat (Miniopterus villiersi ), Mount Nimba, Liberia. Photograph by Ara Monadjem.

specialisation. If this hypothesis were correct, we would predict that closely related species of Miniopterus would differ in habitat, whereas distantly related species would differ in diet. The second hypothesis, with the unhelpful name of ‘General Vertebrate Model’, makes the prediction that closely related species differ in diet, whereas distantly related species differ in habitat (Glor 2010; Streelman and Danley 2003); hence we would make the converse prediction for Miniopterus in Madagascar, namely that closely related species would differ in diet whereas distantly related species would differ in habitat. To test these two hypotheses, Schoeman and his team had to determine the degree of relatedness between all 12 Miniopterus species in Madagascar, and figure out which are most closely related to each other and which are more distantly related. This required constructing a phylogeny, or ‘family tree’, for Malagasy Miniopterus based on DNA sequences.8 The team then modelled the distribution of each species on the island using niche modelling (which is now generally referred to as species distribution modelling or SDM). This is a useful technique that allows one to draw a map of where a species is likely to occur based on environmental variables such as altitude, habitat and climate; in other words, it is a quantification of the Grinnellian niche.9 Quantifying the Eltonian niche is rather 158

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more complicated and requires detailed understanding of, among many other variables, the diets of the different species – information that is still lacking for most Malagasy, and indeed African, bats. As a result, the study used a proxy for diet by considering two features for which they did have information: echolocation call, which allows bats to detect and locate prey; and skull morphology, which allows bats to kill and handle prey. Although to our eyes the skulls and teeth of bats may all appear the same, there is actually an incredible diversity in their shape and size. For example, frugivorous bats typically have more complex molars – defined by a greater number of ridges creating surfaces with greater unevenness, and hence complexity – than insectivorous or omnivorous bats (Santana et al. 2011). This greater complexity allows for more efficient crushing of plant material during the chewing process. Animalivorous bats (those that feed on any form of animal, be it invertebrates or vertebrates) can be further divided between vertebrate feeders with massively enlarged canines and insectivores with more modestly sized canines. Furthermore, insectivores vary in the size of the shearing crests on their molars, with those feeding on insects with hard cuticles having larger crests than those feeding on softer insects such as caterpillars and moths. The results of this study are interesting indeed, because they represent the first time that such a detailed ecological analysis has been conducted for any small mammal radiation in Africa. What the authors found was that closely related species tended to occupy different habitats, as predicted by the Habitat First Rule. They suggested that the ancestral Miniopterus rapidly spread out across the island, occupying available habitats – thus fulfilling the Grinnellian niche model – and diversifying into different species along the way. However, they were not able to demonstrate that during subsequent waves of colonisation species sharing similar habitats diversified into dietary specialists, as would be expected under the Eltonian niche model. They concluded that perhaps a more detailed investigation of the Eltonian niche, rather than the superficial proxy for diet that they used, might be useful in answering this question.

NICHE PARTITIONING AND PLAINS ANTELOPES No chapter on niche partitioning in African wildlife would be complete without a mention of plains ungulates. There are more large herbivorous mammals packed into African savannas than anywhere else in the world. Herbivorous ungulates, 159

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and the predators they attract, are the main drawcard for most nature-based tourists to Africa. A two-day visit to almost any African savanna park will allow easy sightings of up to ten or more antelope species, plus giraffes, warthogs, zebras, elephants and others. You might wonder how so many ecologically similar species can make a living in the same place. To take an analogy from the human environment, it would be like finding a dozen bakeries operating on a single street in a small village. How can the village sustain so many bakeries, when just one would be enough to satisfy the population’s need for bread? The ability of African ungulates to divvy up the resources of a savanna landscape so that all can overcome the competition and find their own place might appear similarly baffling. And many of the world’s best ecologists have dedicated their whole lives to solving this mystery. Zoologists understood early on that African antelope separate into two main feeding guilds: grazers that feed on grass, and browsers that feed on everything else from the botanical world, including the leaves, buds, fruits and woody material of shrubs and trees.10 In ecological parlance, these herbivorous large mammals were partitioning their niche. In the 1970s, this concept was developed by two brilliant ecologists, Peter Jarman and Richard Bell, into what has become the Jarman-Bell Principle (Bell 1971; Jarman 1974). They realised that the diet of an ungulate could be related to its body size, mediated by the universal principles of physics. A small object has a larger surface area in relation to its volume than a larger one. This law of ‘surface area-to-volume ratio’ holds irrespective of what the object might be; it applies as much to rocks as it does to living creatures.11 But how does this relate to animals’ diets? It’s all about the costs and savings of energy. A larger mammal loses less energy proportionately – that is, per unit of its mass – than does a smaller mammal. This is purely because, in the larger mammal, its smaller surface area in relation to its volume means that heat from its body has less chance to escape. Smaller mammals, therefore, are at an energetic disadvantage: they must expend more energy in order to maintain the same optimal body temperature required for efficient metabolic processes to take place. Since small mammals are expending more energy, they will need more energy input – in this case, food – and so smaller mammals have higher metabolic rates than larger mammals. This explains why small mammals are constantly at risk of starving while larger ones are not. For a tiny shrew, missing a meal may spell death. This principle explains the differences in feeding and diet between smaller ungulates and larger ones. A duiker or dik-dik needs to consume proportionately more food than a zebra or buffalo (figures 7.5a–b).12 It is important to 160

(a)

(b) Figure 7.5. a–b. A Kirk’s dik-dik (Madoqua kirki ) (mass ca.6 kg) and an African buffalo (Syncerus caffer) (mass ca.600 kg) as examples of small and large herbivorous mammals. Photographs by Ara Monadjem.

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stress the word ‘proportionately’. Obviously, a large animal must take in more food than a small animal because it has more body to feed. However, proportional to its body size, the larger animal needs less food than a smaller one. A small shrew may consume twice its body mass in a day. That would be equivalent to a zebra eating 500 kilograms of grass during the same period, which it most certainly does not! Let us now apply the Jarman-Bell Principle to explain how African ungulates partition savannas, allowing so many different species to coexist. Because of their higher energy requirements, small-sized ungulates are forced to exploit nutrient-rich foods such as young and growing leaves, fruits and flowers. Larger ungulates, because of their lower energy requirements, can subsist on nutrientpoor foods such as dry grasses. This is the reason why duikers and bushbuck, for example, are browsers, whereas zebras, hippopotamuses and eland are grazers. Within each of these two guilds, we can see further differentiation. For example, in the Kruger National Park, the following grazers occur throughout much of the park: African buffalo, blue wildebeest, plains zebra, sable antelope and common waterbuck – with roan antelope, eland and tsessebe present in the north, white rhinoceros largely in the south, and hippopotamus utilising much of the park at night. However, only rarely will any of these species be seen feeding side by side.13 This is because they are separated on additional niche dimensions. White rhinoceroses and hippopotamuses are megafauna (see chapter 6), weighing well over a ton, and therefore have the lowest metabolic rates of the grazing guild. As a result, they can extract energy from the most nutritionally poor and desiccated grasses on which other antelopes would not be able to survive. Thus, two explanatory variables – the browser versus grazer diet and differences in body size – allow us to elucidate, to a surprisingly large extent, how savanna ungulates are able to coexist. There are, of course, exceptions to this, such as the browsing black rhinoceros, but it is this simplicity that makes the Jarman-Bell Principle so attractive. However, ecology is ‘messy’ and considerations of body size can only get us so far in understanding antelope coexistence. The relationship between body size and diet, although biologically meaningful, is not a perfect association. There are other factors that come into play, factors that are not yet fully understood. Predation, and the associated landscape of fear, is one such factor, and this will need much more research attention in the future. Another factor, which I will discuss briefly here, is diet differentiation. 162

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We have seen how diet divides ungulates broadly into those that ingest grasses and those that feed on other non-grass plants. These are easy, broad categories for an ecologist to record in the field. But what plants exactly is a zebra or buffalo feeding on? Do different ungulates specialise in different plant species? This is not an easy question to answer by simple observation: following wild ungulates with the intention of documenting the plants that they have fed on might appear an almost impossible task. Earlier studies made some headway by following tame, hand-reared, individuals and watching what they ate (Field 1970, 1976; Owen-Smith and Cooper 1987). However, these were hampered by limits in the selection of species that had been tamed and were available for study, the small numbers of tame individuals per species, and problems with interpretation – in other words, can we transfer to wild populations what we learn from observation of a hand-reared animal? And knowing the grass species being grazed upon is only part of the answer. In principle, two species of antelope grazing in the same area on exactly the same grass species need not be directly competing with each other. This is because they may be selecting different parts of the grass. One species may be feeding on the green leaves, which have higher nitrogen content, while another species may be nibbling on the dry stems, which are coarser (Sinclair 1977). This has obvious implications for niche partitioning. One other point needs a brief airing here. There is convincing evidence to suggest that different ungulate species, far from competing with one another, may in fact facilitate one another’s presence. This was recognised back in the late 1950s by research conducted in the Rukwa Valley in south-western Tanzania (Vesey-FitzGerald 1960), the dominant feature of which is Lake Rukwa, a saline body of water that varies greatly in extent from year to year – although there is fear that it is now in danger of drying up altogether. Here, elephants first trampled and grazed the tall grasses growing on the floodplains around the lake, creating open patches. They were followed by buffaloes that continued to trample and graze these patches down, eventually allowing topi (Damaliscus lunatus jimela, figure 7.6), a short grass specialist, to forage these patches.14 In other words, without elephants and buffaloes, the topi could not have accessed the nutritious grasses surrounding much of the lake. The concept of facilitation has been greatly developed since then, including the recognition that grazing lawns (McNaughton 1984; Waldram et al. 2008), which are such magnets for plains antelope across the continent, have been created and maintained by 163

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Figure 7.6. Topi antelopes (Damaliscus lunatus jimela) grazing in the vicinity of the Maasai Mara National Game Reserve, Kenya. Photograph by Ara Monadjem.

other ungulates. For example, the large migratory herds of wildebeest in the Serengeti (see chapter 8) seasonally reduce the amount of grass available at any location by up to 85 per cent during the few weeks that they are present (McNaughton 1976). Contrary to what one might expect, this vastly improves grazing conditions for the 550 000 Thomson’s gazelles (Eudorcas thomsonii) that appear on these same grazed plains a month later. Returning to our original question of how to identify which plants herbivorous mammals are feeding on, we find molecular biology can help us out. We have already seen how molecular techniques have been employed to answer all sorts of evolutionary questions, such as resolving species boundaries (taxonomy). They have also addressed ecological questions, such as what exactly different antelope species feed on. A recent study showed that ungulates inhabiting an arid savanna in Kenya fed on entirely different groups of plants (Kartzinel et al. 2015). Tyler Kartzinel and his colleagues collected faeces from four antelope species, two species of zebra and the savanna elephant, from which they then extracted and sequenced DNA from the plants ingested by the animals. They demonstrated that each ungulate fed on a wide variety of 164

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plant species, generally within the broad guild of browsers or grazers (or mixed feeders) to which it had traditionally been assigned. However, the interesting finding was this: even though each species was found to have a broad diet, there was little overlap in diet between one species and the next – even between those in the same feeding guild. Although the use of molecular techniques to quantify the diet of mammals is a rather new field, other laboratory-based methods have been employed to investigate similar questions. In particular, the use of stable isotopes has been popular among ecologists (McKechnie 2004). This technique requires a high-tech laboratory, but the principles are relatively easy to understand. Many elements naturally exist in slightly different configurations, according to the number of neutrons an atom has in its nucleus. Thus an element such as carbon (C) can come in the standard configuration with 12 neutrons or with an additional 13th neutron. These variants are called isotopes of carbon and are presented as 12C and 13C, respectively. With the right tools and machinery, we can measure the ratio of these two isotopes in living organisms.15 Because an animal obtains carbon from its food, we would expect the ratio of 13C to 12C in its tissues to reflect the ratio found in the food that it ingests. Mammals, or any other animals, that share a similar ‘signature’ – that is, that have a similar ratio of the two isotopes – are assumed to be feeding on similar foods, while those that have divergent signatures must be feeding on different ones. In theory, we could use any elements with isotopes for our analyses, although biologists interested in dietary studies have tended to focus on carbon and nitrogen (N) (Crawford et al. 2008). A more critical consideration, however, is the choice of tissue from the mammal that we select for study. Different tissues have different turnover rates, depending on their nature. Bone, for example, takes months to lay down. Thus, extracting bone tissue may provide a window on what the mammal fed on in a previous season or a previous year. In contrast, blood has a far quicker turnover time, allowing us to reconstruct what the mammal was feeding on over the past few days. Keratin – as found in hair or claws – lies somewhere in between and can allow us to gauge what was consumed during the past few weeks. Stable isotope analysis provides only an indication of how similar or divergent the diets of different animals are. It cannot be used to distinguish finescale differences, like those achieved with molecular sequencing in the Kenyan arid savanna study. However, it can address dietary questions on a broad scale, 165

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and has been successfully employed to determine niche overlap in west African savanna antelope at Pendjari Biosphere Reserve in Benin (Djagoun et al. 2016). This ungulate community comprises 11 species, of which 4 are browsers and the rest grazers, ranging in size from about 12 kilograms in 2 species of duiker to more than 600 kilograms for the African buffalo (Syncerus caffer). As expected, the study found a lot of overlap in isotopic signatures between different species, partly because of significant variability within each species. Furthermore, there were also seasonal differences. However, the authors demonstrated that the mean overlap of isotopic signatures between species was lower than expected by chance, which they concluded was a sign of niche partitioning in this herbivore community.

STABLE ISOTOPES AND SMALL MAMMAL COMMUNITIES Stable isotope analysis has recently been used to demonstrate similar niche separation in terrestrial small mammal communities in South Africa (Codron et al. 2015; Symes et al. 2013).16 Since small mammals as a group have a larger dietary breadth than plains ungulates – because their diets include not just plants but also animals, and animals that prey on other animals – stable isotope analysis has been especially useful in distinguishing niches that can provide separation on two axes (figure 7.7). The one axis involves 13C-to-12C (carbon) ratios that typically indicate a separation between grazers and browsers – or from a small mammal perspective, the distinction between grassland and forest dwelling. The other axis involves 15N-to-14N (nitrogen) ratios that can distinguish between animalivorous and herbivorous species – nitrogen is essential for building proteins, which differ in animals and plants. Craig Symes, a respected ornithologist formerly from the University of the Witwatersrand in Johannesburg, South Africa, but now based in New Zealand, used stable isotope analysis to examine niche partitioning in a small mammal community inhabiting a grassland–forest mosaic. Working with several colleagues, he was able to show that the small mammal community, comprising eight species, was partitioned along the two stable isotope axes referred to above. Furthermore, his study was able to deduce that grassland species were generalists with broad dietary niches, whereas forest species had more restricted dietary niches, which suggested specialisation (Symes et al. 2013). 166

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14

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12 10 8 6 –26

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Figure 7.7. A graph showing the differences in diet of two groups of bats based on stable isotope analysis. The horizontal axis shows the values of the carbon isotope while the vertical axis shows the nitrogen values. Each symbol (circle or triangle) shows the diet of a single individual bat. The circles are located to the left of the triangles, indicating that the diet of these bats is mostly from forested environments, compared with grassland environments for the bats represented by triangles. However, in terms of trophic level, the two groups cover similar ranges on the vertical axis.

An additional interesting observation was that the arboreal rodents had higher 15 N-to-14N ratios, like those of shrews, signifying that there must be more animal protein in their diets than had previously been documented. Similar conclusions were reached by another recent stable isotope analysis conducted north of Johannesburg in Gauteng Province by Jacqueline Codron and her colleagues (Codron et al. 2015). This study included ten small mammal species across three habitats: grasslands, woodlands and marshes. As in Symes’s study, these researchers found niche separation between species that occupied the same habitat. They also demonstrated that species with a high dietary niche overlap – for example the striped mouse (Rhabdomys pumilio) and the Namaqua rock mouse (Micaelamys namaquensis) – occupied distinctly different habitats, with the former living in grassland and the latter in rocky outcrops.17 A final example of how stable isotopes can help to shed light on ecological issues comes from a collaborative study that I was involved in. We wanted to address the question: how do tropical communities support 167

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a greater number of species than subtropical ones? We chose bats as our study group, and compared the community composition at Mount Nimba, a tropical rainforest in west Africa, with that in the Soutpansberg mountains, a subtropical savanna in South Africa (Monadjem et al. 2018). I had been working at Mount Nimba for many years and had captured most of the bat species the mountain has to offer, while Peter Taylor (whose work I referred to in chapters 1 and 5) had a similar collection from the Soutpansberg. Ecologists and biogeographers have known for a long time that tropical rainforests are super-diverse, but why this should be the case remains an open question. Ultimately, this is the question that ecology needs to answer, but our study was far more modest in its goals. We figured that if we could address the issue of how the rainforest is able to support more species than the savanna, then perhaps this could shed light on the bigger question of why it does so. A total of 59 species of bat have now been recorded from Mount Nimba, which is one of the most important hotspots for bats in Africa (Monadjem et al. 2016). By contrast, 45 species are known from the Soutpansberg (Taylor et al. 2013), which covers a far larger area. For each of the two sites, we measured the shape of the skull and teeth of the bats occurring there – as a proxy for what the bats might be feeding on – and we ran stable isotope analyses on carbon and nitrogen from fur clippings. Based on the morphological analysis (examining the skulls and teeth), we were able to show that the bat community at Mount Nimba occupied a larger area in ‘morphospace’ than the one in the Soutpansberg mountains.18 In other words, the size and shape of skulls and teeth in the tropical rainforest bats displayed more variation than in the savanna. Interestingly, this difference disappeared when we removed fruit-eating bats from our analysis and examined only insect-eating bats. From this, we concluded that the rainforest bats were exploiting a wider range of niches than savanna bats, mostly because the rainforest harboured a greater diversity of fruit bat species. The stable isotope analysis, on the other hand, showed clear separation between rainforest and savanna bats. Both bat communities had a similar range of nitrogen isotope ratios but they differed in the carbon isotope ratios. These examples serve to demonstrate the value of applying such ‘high-tech’ techniques to ecology.

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*** In this chapter, we have looked at how communities of plants and animals are organised. We started by looking at two divergent interpretations of how plant communities are formed: Clements’s super-organism versus Gleason’s individualistic responses of species. We saw that these ‘communities’ appear organised and structured but in fact comprise discrete species that respond individualistically to environmental and biotic variations in their landscape. We then looked at how zoologists have tackled this issue by defining Grinnellian and Eltonian niches. The former emphasises the geographical properties of the distribution of a species, while the latter emphasises the biotic interactions within and between species. We used the concept of niche partitioning to explain the coexistence of various African mammalian communities, including the super-diverse communities of large mammalian herbivores and bats. In the next chapter, we will look at the factors that influence species abundance.

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8

Fluctuating Populations

S

o far, we have not really considered how the size of a species’ population contributes to its distribution. Yet populations of most species fluctuate in size from year to year depending on factors such as rainfall. In chapters 3, 4 and 5 we looked at how species have expanded and contracted their ranges as they have negotiated barriers, such as oceans and mountains, or tracked shifting habitat. We did this explicitly from an evolutionary perspective. In this chapter, we will see that populations of species also expand and contract in ecological time. It all boils down to just four simple factors: births and immigration, which increase an existing population; and death and emigration, which reduce it. However, unpicking how these four factors operate in an ever-changing environment is anything but simple, as we will see. Understanding what factors drive the population dynamics of animals is important for several reasons. For one thing, managing populations of large, wild mammals – whether for conservation, meat production or hunting – requires us to maintain populations at ‘optimal’ levels so that we can, for example, maximise yield. There are also theoretical reasons for wanting to study population dynamics. For example, if we imagine a species that is widely distributed and abundant in more than one habitat, we tend to assume that it is doing well in an ecological sense. However, it could be that this species only thrives in one habitat (called the ‘source’), from which it colonises the adjacent habitat (called the ‘sink’). Such source–sink dynamics can profoundly influence the functioning of any ecosystem (Battin 2004).

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HOW LIFE HISTORY AFFECTS POPULATIONS A good place to start understanding population dynamics is life history. We all easily recognise differences between a mouse and a buffalo on morphological grounds: the former is small and furry, with continuously growing incisor teeth; the latter is much larger, with horns, hooves and no upper incisors at all. These differences may be interesting from a systematist’s perspective, allowing us to comment on the evolutionary relatedness of different groups – although as we saw in chapter 2, molecular techniques have more or less taken over from morphological studies in this respect. However, to an ecologist, particularly a population ecologist interested in the fluctuations in an animal’s numbers, life history traits are key. These can be defined as features of an organism that affect its population numbers, and include such factors as reproductive output, developmental growth rates and survival rates. To return to our earlier example, a mouse may give birth each year to several litters of five or six young, which develop rapidly and themselves give birth within months of being born. A buffalo, on the other hand, gives birth to a single offspring that takes several years to reach maturity. Without even doing any mathematics, it is clear that the population growth trajectories of these two species will be radically different: a mouse population, given unrestricted access to food, will multiply rapidly, whereas a buffalo population will increase at a much slower rate. These two animals thus fall at opposite extremes of the spectrum of life history strategies exhibited by mammals. This brings us to what ecologists know as r/K-selection. Mammals that focus their energies on producing large numbers of offspring generally do so at the expense of their own survival. Species exhibiting these traits typically reach sexual maturity in a matter of weeks or months and rarely survive beyond a year or two. This strategy is exemplified by the multimammate mouse (genus Mastomys). A female can give birth to a litter of more than a dozen pups and produce several litters in a season. The pups can reach sexual maturity, and hence mate, within 2 months, and give birth to their own pups approximately 23 days later, but as adults rarely survive more than a year. By contrast, the Cape buffalo (Syncerus caffer) typically gives birth to just a single calf, after an 11-month gestation period, per year (figure 8.1). This calf takes up to 5 years to reach sexual maturity, but may go on to live up to 20 years in the wild. In crude terms, the mouse invests in quantity: it produces many offspring, only a few of 171

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Figure 8.1. A herd of buffalo (Syncerus caffer) showing at most one calf associated with each cow. Photograph by Ara Monadjem.

which will survive, whereas the buffalo invests in quality: it raises (as opposed to simply produces) only a smaller number of offspring but devotes more time and care to their upbringing, ensuring that a larger proportion will survive, and will go on to live much longer. These two contrasting life history strategies are known, respectively, as r-selection and K-selection.1 Species that invest in quantity, such as the multimammate mouse, are described as ‘r-selected’, while those that invest in quality, such as the buffalo, are described as ‘K-selected’. However, r- and K-selection are not merely terms that describe the population growth capacity of different species; they also encapsulate the different environments in which these different capacities can function. For example, r-selected species, such as the multimammate mouse, prosper in unpredictable or variable environments, where, for example, food is super-abundant at unpredictable times or for variable lengths of time. By contrast, K-selected species, such as the Cape buffalo, do better in stable environments, where food supply is more predictable. Note that the ‘environment’ here can be radically different 172

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for two species occurring at the same geographical location, because they may differ in what they consume, where they roost and so on. The environment, therefore, is not simply a catalogue of, say, climatic conditions, although climate may influence certain resources such as food supply. Rather, it is the niche of the animal concerned (as discussed in chapter 7). Hence, life history strategies allow us to understand why organisms vary with respect to their reproductive output and survival. They explain why some species produce lots of offspring and others do not; why some species fiercely protect their offspring, to the point of risking their own lives to ensure their survival, and others do not; why some species die after only a few months of adulthood while others live for decades. Ultimately, it is all about how many descendants you produce that themselves survive to produce further progeny, in a perpetual cycle, and there are many different ways in which this can be achieved. The r-selected and K-selected strategies are two alternatives at opposite ends of a continuum. Between them, intermediate strategies also exist. Reproduction and survival We can examine the variety of life history strategies available to mammals by looking at a community of rodents occurring in a savanna system. A typical grassy savanna in southern Africa supports about 10 to 20 species of rodent. The majority belong to two diverse families, the Muridae and Nesomyidae – the ‘classic’ rats and mice. Other families include the squirrels (Sciuridae), porcupines (Hystricidae), cane-rats (Thryonomyidae) and mole-rats (Bathyer­ gidae), with dormice (Gliridae) occurring in more wooded situations. If we examined just the rats and mice, which are generally smaller and more readily enter various live-traps put out by biologists, we would not be surprised to record the following genera: multimammate mice (Mastomys), striped mice (Lemniscomys), veld rats (Aethomys), rock mice (Micaelamys), pygmy mice (Mus), gerbils (Gerbilliscus), vlei rats (Otomys), fat mice (Steatomys), climbing mice (Dendromus) and pouched mice (Saccostomus, figure 8.2). Litter sizes vary between species, with vlei rats generally having the smallest (around two to three pups per litter) and multimammate mice having the largest (regularly more than ten pups per litter). However, there is considerable variation within genera and even within species. The largest litter recorded for a vlei rat is 5 (Phillips et al. 1997), whereas the mean litter size of the normally super-fecund multimammate 173

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Figure 8.2. A pouched mouse (Saccostomus campestris). Photograph by Ara Monadjem.

mice in a study in Senegal was just 6.5 (Duplantier et al. 1996).2 Thus, the fecundity of a species may vary geographically with changes in resource availability. Even at a fixed location, females in better condition will give birth to larger litters. This variability, which is inherent in all biological systems, is often lost when we report mean values, which is why scientists include the standard deviation – a measure of the variation around the mean – when presenting an average value. However, even taking into account this variation, it is clear that some species are more fecund than others because of the possession of one or a combination of the following: earlier sexual maturation, larger litter size, faster growth rate, shorter gestation period and shorter interval between successive births. Were we to arrange our ten aforementioned rodent genera in order of productivity, from most to least, we would be able to identify four categories: superfecund (Mastomys and Mus), highly fecund (Gerbilliscus, Lemniscomys and Saccostomus), intermediately fecund (Aethomys, Micaelamys, Dendromus and Steatomys) and lowly fecund (Otomys) (table 8.1). If we were to arrange these 174

Table 8.1. Life history traits of some common southern African rodents in the families Muridae and Nesomyidae.

Species

Gestation Mean Mass (g) period (days) litter size

Age at weaning (days)

Minimum age at first reproduction (days)

26

82

Aethomys ineptus

78

26

3.1

Dendromus melanotis

9

23

3.6

Gerbilliscus leucogaster

72

28

5.4

28

Lemniscomys rosalia

58

24

6.5

20

Mastomys natalensis

41

22

9.5

21

Micaelamys namaquensis

48

23

3.4

26

Mus minutoides

7

19

4.0

Otomys angoniensis

114

37

Saccostomus campestris

50

21

Steatomys pratensis

24

Minimum interval between litters (days)

Maximum longevity (months)

12–14 77 (54)

24

12

18

42

22

12

3.1

16

80–100

6.7

22

96

Sources: Mass taken from Monadjem, Taylor et al. (2015). Remaining characteristics taken from Neal (1990), Phillips et al. (1997) and Happold (2013).

24

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same genera by length of survival, we would reverse the order, with Otomys surviving for two or more years in the wild, Mastomys and Mus surviving only for a few months – or up to a year in the longest-lived individuals – and the remaining genera fitting somewhere in between.3 We could, therefore, place all these rodents on the r/K-selection continuum, with Mastomys/Mus towards the r-selected end and Otomys nearer the K-selected end. How would this tie up with what we know about the niches of these rodents? The vlei rats (Otomys) feed on green plant material, particularly the leaves and stems of grasses and herbs. The supply of this food source is relatively constant and stable between seasons and years in the habitats they favour, which include wetlands and moist grasslands. By contrast, multimammate mice (genus Mastomys) are unable to maintain body condition on green plant material alone, so are more generalist feeders, selecting nutritious grass seeds and insects and increasing their consumption of green plant material only when other foods are unavailable (Monadjem 1997). Their food supply varies significantly, between both seasons and years, because grass seed yield is closely tied to rainfall, which can be highly unpredictable. Lemniscomys has a diet that is somewhat intermediate between Otomys and Mastomys, taking mostly green plant material but also including grass seeds. There is thus a close association between the niches of these rodents and their life history strategies, as predicted by r/K-selection theory (Willan and Meester 1989). Although r/K-selection theory is today generally thought to be too simplistic a concept to answer all questions in this field (Reznick et al. 2002), it can still prove useful in helping us think about the relationship between an animal’s niche and its life history traits. Immigration and emigration How does all this relate to population dynamics, the subject of this chapter? The link is clear if we consider the four factors that determine populations. So far we have dealt with two of them – births (reproduction) and deaths (survival) – and related them to life histories. The remaining two factors, immigration and emigration, can also be linked to life history traits, but through the process of dispersal. Dispersal refers to the movement of animals – typically young ones – from their natal grounds (places of birth) to where they settle down to breed and live out their lives. For example, the vlei rat (Otomys auratus) has been shown to disperse an average of just 11 metres from its place of birth – typically 176

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a grass nest on the surface – to the centre of its adult home range. The dispersal distance of the striped mouse (Lemniscomys) is not known, but in the closely related genus Rhabdomys, individuals have been shown to disperse an average distance of 83 metres (Willan and Meester 1989) between natal grounds and adult home range. The dispersal distance in Mastomys is even further (Leirs, Verheyen and Verhagen 1996; Russo et al. 2016; Van Hooft et al. 2008). Hence, K-selected animals typically remain ‘at home’, often taking over the territories of their parents, whereas r-selected animals are flexible and may move large distances to reach suitable sites, away from their parents. Thus far in this discussion of population dynamics we have seen that mammals have different life history strategies, and these are closely associated with their niches. Ultimately, it’s about how species expend energy in the reproduction process, with r-selected species expending their energy more intensively and thus over a shorter time period. K-selected species typically dominate stable environments, while r-selected species dominate environments where conditions are less predictable. Finally, r-selected species are typically generalist (think ‘weedy’) species, capable of feeding on diverse foods, and are flexible in when and where they breed. K-selected species, on the other hand, are typically specialists that, for example, feed on a restricted type of food or harvest it in a specific way, and are inflexible in when and where they breed. These contrasting life histories generate distinctly different population dynamics, as we will see in the next section.

POPULATION DYNAMICS AND RODENT OUTBREAKS Except on well-managed farms, animal numbers do not remain constant over time; and even on farms, domestic livestock numbers may fluctuate – declining during a drought, for example. As a result, the population size of a particular species in a particular area varies from year to year, often in sync with its food supply but also affected by predation and extreme weather events. In years following good rains, the populations of herbivorous and omnivorous mammals tend to increase as their food supply increases, resulting in higher rates of recruitment as more young animals survive to join the adult population. In contrast, during drought years the populations of carnivores and scavengers increase as their prey, typically herbivorous species, are increasingly 177

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Population size

stressed by the declining quantity and quality of graze and browse, and become easier targets for predation. What interests us at this stage is that the rate of change of a population is affected by its life history traits. Populations of r-selected species have higher potential growth rates than those of K-selected species (figure 8.3). This is hardly surprising: a species that matures rapidly, has large litter sizes and gives birth to new litters at short intervals will, self-evidently, have populations that grow more swiftly than a species whose life history traits are the opposite of these. Classically, r-selected species such as many rats and mice show enormous fluctuations in their populations, in contrast to K-selected species such as elephants. Again, we can take as an example multimammate mice (figure 8.4), which have been studied extensively across Africa. In a typical savanna, the numbers of these rodents can oscillate in a matter of months between lows of close to zero animals and highs of several tens of animals per hectare (Monadjem and Perrin 2003). Numbers can build up to even higher densities

Time

Figure 8.3. A hypothetical graph showing the contrasting trends of population growth of an r-selected compared with a K-selected mammal. In the case of a K-selected species (stippled line), its population typically increases gradually until it reaches an asymptote, after which it remains relatively stable. In contrast, the population of an r-selected species (solid line) typically rises and drops quickly, and rarely remains stable at any point in time.

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Figure 8.4. A Natal multimammate mouse (Mastomys natalensis). Photograph by Ara Monadjem.

in agricultural fields, sometimes exceeding 400 animals per hectare (Leirs and Verheyen 1995). Compare this with, say, populations of elephants that typically grow at around 3 to 5 per cent per annum (Moss 2001) under favourable conditions, but at up to 10 per cent when introduced to areas lacking elephants, such as newly created parks and reserves (Mackey et al. 2006). Thus, without an influx of elephants from a neighbouring population, we will hardly notice changes in numbers from one year to the next. Even at a 10 per cent growth rate, a population of 100 elephants will increase to just 110 animals in the following year. Compare this with a population of 100 multimammate mice that could, under favourable conditions, easily increase to more than 1 000 individuals in the same period – and then decline to just a handful of individuals a few months later. Long-term, multi-year studies of African rodent populations are rare. The most famous dataset deals with the population of multimammate mice and other species associated with maize fields around Morogoro, Tanzania. This 179

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study commenced in the early 1980s and has been continued, almost without a break, right up to the present, covering more than three decades of intensive trapping. In chapter 9, we will look in greater detail at the Morogoro study and its main protagonists, Herwig Leirs and Rhodes Makundi. For now, we just need to know that this qualifies as one of the most outstanding studies on African rodents. What it makes clear is that rodent numbers increase and decline on a predictable seasonal basis, peaking during the early wet season, October–December, and reaching their lowest numbers in the June–August dry season (Leirs and Verheyen 1995). In Morogoro, the wet season may last from October to May, but is usually bimodal during this period, as we will see later in this chapter. This is followed by a long dry season that lasts until September. Multimammate mice typically breed during the wet season, starting when the rains begin that trigger new plant growth and thus a greater food supply. In Eswatini, populations of rodents also follow a predictable interseasonal pattern, with lowest densities occurring at the beginning of the wet season, in October– November, and highest densities at the end of the wet season, in April–May (Monadjem and Perrin 2003). This, in fact, is the typical pattern for rodent populations across southern African savannas. However, while the seasonal pattern may be predictable, the amplitude of its fluctuations is not. Peak densities in one year may be several times higher than in the previous year. And the pattern only becomes discernible when one examines, and averages, several years of data. Having ‘unseasonal’ peaks is not at all uncommon. One other notable aspect of the population ecology of multimammate mice is their capacity for population outbreaks. In these ‘boom’ periods, when the population peaks at extremely high levels, the rodents can wreak havoc on crops and spread diseases to humans (see chapter 9). Forecasting such outbreaks is thus of great agricultural, economic and social importance. However, they do not follow a regular pattern. In another long-term, but not continuous, study in the Serengeti ecosystem, Andrea Byrom and her colleagues reported nine outbreaks between 1968 and 2010, occurring at three- to five-year intervals (Byrom et al. 2014). The outbreaks followed ‘good’ rainy seasons, and were followed 6 to 12 months later by an increase in the populations of predators feeding on these rodents, including the black-shouldered kite (Elanus caeruleus) and various small mammalian carnivores such as jackals, genets and mongooses. The most elaborate rodent forecasting model, which we will consider later in this chapter, has been developed by Leirs and his collaborators. Working with the Morogoro 180

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dataset, they showed that outbreaks were statistically predictable, based on the amount and timing of rainfall. But before we examine the nature of this relationship, we need to understand the importance for population studies of accurately determining rodents’ ages. The importance of knowing the ages of rodents Populations are not homogenous: they consist of males and females, and various age groups, from juveniles to adults. Sexing rodents can be tricky, especially for juvenile and subadult individuals, as the penis is not usually externally visible, and the testes only descend in breeding males. Nonetheless, with a little field experience it is generally possible to distinguish males from females, for example by examining the distance from the urinary papilla to the anus (long in males because this is where the testes will descend, but short in females). Ageing rodents is a different matter entirely, however, and knowing the precise age of a rodent is a critical parameter in any population model. Various methods have been proposed or used by mammalogists to age rodents. These include examination of the pelage (coat), which is typically softer in juvenile mammals; of the body mass, with adults being heavier than juveniles; and of the extent of tooth wear, with adult teeth typically more heavily worn than those of juveniles. However, these methods are not precise and cannot be used to accurately gauge the date of birth of the individual. Another technique that has been more successfully employed is that of measuring eye lens weight, since the lens continues to grow throughout the life of a rodent. Leirs used this method to age multimammate mice in the Morogoro study. He also employed it to show that the population age structure changes through the year, with the proportion of adults in the population increasing during the breeding season and reaching a peak in May–August, then falling to its lowest proportion at the beginning of the wet season in October–December. He was able to show that juveniles are recruited into the population at the end of the rainy season, which coincides with the species’ breeding season. The adults then perish, leaving behind a population mostly comprising the recently recruited youngsters that grow into the next generation of adults in the subsequent breeding season. What, then, causes population outbreaks in multimammate mice? We have already seen that there is a relationship with rainfall: outbreaks always follow years with high rainfall. However, not all good rainfall years are followed by 181

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outbreaks. In the mid-1980s, Lynnwood Fiedler successfully predicted an outbreak in Chad and Sudan (now Sudan and South Sudan), during the 1986–1987 season (Fiedler 1988). He based his forecast on the fact that several years of drought had been broken by good rains in the 1985–1986 season. His reasoning was that the severe drought would have reduced not only rodent populations but those of other herbivores, such as antelope, too. In addition, the populations of rodent predators would have plummeted. Because multimammate mice – and other similar rodents – are r-selected, he predicted that their populations would now rebound more rapidly than their antelope competitors feeding on the same grasses, particularly in the temporary absence of predation. Rodent outbreaks elsewhere in Africa have also followed prolonged droughts directly preceding good rains. This was the case in Botswana and Kenya in the 1960s and across the Sahel, which extends from Senegal to Sudan, in the 1970s. However, rodent irruptions do not follow after every prolonged drought, and some outbreaks have occurred without even a single drought year preceding them. Hence, there does not appear to be a specific relationship between years of high rainfall following drought years and rodent outbreaks. This relationship is more complex than can be explained simply by tracking rainfall, and outbreaks are difficult to predict with precision – or, at least, we need to recognise that there are regional differences in the mechanisms driving rodent outbreaks. For example, in east Africa, Leirs and his colleagues have convincingly shown a strong link between rainfall – particularly the timing of rainfall – and irruptions, but they failed to demonstrate a similar link between droughts and irruptions (Leirs, Verhagen et al. 1996). All outbreaks occurred after good rains, but they specifically noted that when good rains fell in the early part of the wet season, around October–December, the chances of an outbreak were significantly increased. The reason is rather simple. Rainfall in much of east Africa is bimodal, falling in the early part of the wet season as the ‘short rains’ in October–December, or towards the end of the wet season as the ‘long rains’ in March–May. The long rains are for the most part reliable, but the short rains range from being almost entirely absent, as in 1993, to being as heavy as the long rains, as they were in 1982 and 1988. As we saw above, rodent numbers reach their peak in the short rains period. Therefore, if these rains are poor, rodent numbers decline rapidly, presumably because of shortages of food, which for multimammate mice consists primarily of plant material. If, however, the short rains are heavy, then the already high rodent population gets a further boost, 182

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allowing it to reach densities typical of an outbreak, as happened in 1983 and 1989. By now it should be clear that r-selected and K-selected species exhibit vastly different population dynamics, with the former showing large fluctuations in numbers from season to season and year to year, while the latter change far less dramatically. Earlier I compared a mouse with a buffalo, perhaps suggesting that small animals are r-selected and larger ones K-selected. In fact, this is not necessarily the case. Within small-bodied rodents, for example, some are more K-selected than others (as illustrated by the comparison of Mastomys and Otomys above), and among ungulates some are more r-selected than others; and these differences may have nothing to do with body size. For example, some small mammals exhibit life history traits that are more like those of largesized and K-selected mammals than those of other r-selected small mammals. Bats are a case in point, and their story is told next.

BATS AS THE ULTIMATE K-SELECTED MAMMALS We have all heard somebody refer to a bat as a flying mouse, but the comparison is a poor one.4 Not only are the two groups unrelated in an evolutionary sense – their respective lineages having diverged more than 70 million years ago – but they also could not be more different in life history traits. Rodents are short-lived, have short gestation periods, give birth to multiple litters of four or more pups in a year, and grow so quickly that they may breed within weeks of birth. Bats, by contrast, may survive for decades, have a gestation period that may extend up to six months, produce typically just one or two litters of a single pup per year (some species occasionally having twins), and grow much more slowly – females not having their first pup until they are one or two years old. Bats, emphatically, are not flying mice! African rodents have been relatively well studied by a host of researchers across the continent. As a result, we know a little about the ecology of some species, but for the large majority of rodents we possess only a few scraps of biological data. However, when we compare the situation with what we know about the continent’s bats, rodents appear to be a veritable mine of information. As far as I know, for example, we have detailed data on survival for just one species of African bat, the common (or Egyptian) slit-faced bat (Nycteris thebaica, figure 8.5) 183

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Figure 8.5. An Egyptian slit-faced bat (Nycteris thebaica). This species that gives birth to just one pup per year. Note the very large ears that this bat uses to locate prey moving on the ground by sound. Photograph by Ara Monadjem.

(Monadjem, McCleery and Collier 2015). And to the best of my knowledge, we have yet to study the population dynamics of a single species. This difference in our knowledge of demographic and population dynamics between bats and rodents is partially explained by the difficulties of studying bats in the wild. We can easily capture, and release unharmed, large numbers of rats and other rodents using, for example, Sherman live traps. We can set these traps up in a systematic grid formation, and repeatedly capture the same individual rats, enabling us to calculate certain demographic parameters such as monthly survival. Traps are typically baited in the afternoon and checked early the following morning, making for straightforward if somewhat tedious fieldwork. Bat work, on the other hand, involves setting up nets, which are finicky and easily damaged. A single net can take an hour to erect and may catch nothing at all. In the same amount of time, your colleague could have set up 100 Sherman traps in a 10 × 10 grid! The bat worker must then stay up late into the night, fighting off mosquitos and sleepiness. And once an individual bat has been 184

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captured it is rarely recaptured in the same net, presumably because it learns to avoid the site, making it difficult to estimate survival rates or other demographic features. However, the problem also partly has to do with the negative attitudes towards bats shared by so many cultures. Rats may be reviled, but bats are often feared. As a result, we are happy to kill the former, but would rather avoid the latter altogether. Common slit-faced bats are small (weighing about 11 grams) but widespread in the savannas of Africa, roosting during the day in caves and other darkened sites, such as abandoned cellars and mine adits. They frequently roost in culverts that conduct water under roads, and in north-east Eswatini I monitored one population of a few hundred individuals that roost in a dozen or so culverts under a short stretch of the tar road connecting the main entrances of Mbuluzi Game Reserve and Mlawula Nature Reserve. I started capturing and banding them, with a specially designed bat ‘ring’ that fits over the forearm, in 1998 and continued, twice a year, until 2007. In the course of that decade, I banded 1 450 individuals that were recaptured, collectively, almost 1 800 times (Monadjem, McCleery and Collier 2015). Two individuals that I initially captured as adults in 1998 and 1999 were still alive in 2007, an indication of how long-lived these bats can be. And this is as nothing compared with the longevity record for a bat, which is 41 years in a free-living Brandt’s bat (Myotis brandtii) banded and released in 1962 in Siberia, Russia (Podlutsky et al. 2005). A further 67 individuals of this species (from 1 544 bats banded) survived at least 20 years. These are very impressive statistics for an animal weighing just 6 grams. Based on the data that I amassed, we were able to calculate the annual survival rate of common slit-faced bats in Eswatini at about 39 per cent for juveniles and 67 per cent for adults, with males out-surviving females. I say ‘we’, but I should really thank Bret Collier from Louisiana State University in the United States, a co-author of the study, who is an ecologist and a statistical wizard all in one and conducted this analysis. The survival rates quoted above represent the probability of an individual surviving a year. So, when I say that adults had a survival rate of 67 per cent, I mean that 67 per cent of the adults alive in a given year will still be alive 12 months later. For example, if we start out with 100 bats in January, 67 of these bats will still be alive and well in December and 33 will, of course, be dead. Juveniles have far lower survival rates, showing that the first year of life is difficult to get through, but those that make it to adulthood are likely to survive many years after that. Interestingly, this is similar to the typical 185

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survival rates of small songbirds such as robins, thrushes and flycatchers, but it is an order of magnitude higher than that of similar-sized rodents.

AFRICAN ANTELOPES AND POPULATION REGULATION No chapter on population dynamics of African mammals can be complete without a mention of antelopes. Ecologists have devoted much more attention to the population ecology of numerous African antelope species than they have ever done to small mammals. This may reflect the fact that antelope are valued game species that have been hunted for meat, hide and trophies for well over a century. Understanding their population dynamics, therefore, is not solely an academic pursuit but has a strong practical component because it allows us to manage their numbers. Compared with rodents, antelopes have slow rates of population growth and relatively high rates of survival. Most antelope species give birth to a single offspring that will take several years to reach sexual maturity, and adults may survive for a decade or more. In ecological terminology, antelopes are highly K-selected, like their close relative the African buffalo, with populations that fluctuate far less dramatically than those of rodents. This brings us to the last topic that I will discuss in this chapter, that of population regulation and density-dependent factors. What regulates the numbers of animals in a population? This depends on where the species lies on the r/K-selection spectrum. Multimammate mice and other r-selected species have populations that grow rapidly when conditions are good, particularly when food supply is abundant and predation pressure is low. And populations crash following periods of inclement weather when food supply is reduced, such as after a drought in the case of herbivorous mammals. However, the numbers and density of animals in a population will also have an effect, because the more animals there are, and the more densely they are distributed, the more mouths there are that need to be fed in a given area, and the quicker the food from that area will be harvested. This is called density dependence (Sinclair and Pech 1996). Density-dependent factors operate on populations as a kind of negative feedback mechanism, reducing growth rates when the populations are high and increasing them when populations are low. Density dependence curbs growth rates in one of two ways, either by increasing 186

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mortality or by reducing fecundity as the population density increases. The theoretical outcome is that the population is ‘regulated’ or maintained at or around an equilibrium point that is termed the ‘carrying capacity’. In practice, however, this carrying capacity is rarely if ever reached, because of the continuously changing nature of the environment (Sayre 2008). Population regulation in African antelopes has been studied most intensively in two distinct areas: the Serengeti National Park in Tanzania and the adjoining Maasai Mara National Reserve, Kenya; and the Kruger National Park in South Africa. These two magnificent, protected areas provide contrasting insights into how African savanna ecosystems might have functioned before the rise of modern civilisation. Despite many similarities between the two habitats, antelopes in these two ecosystems exhibit vastly different population dynamics. The Great Limpopo Transfrontier Park, of which Kruger is part, covers more than 37 000 square kilometres, while the Serengeti Biosphere Reserve, together with the Maasai Mara National Reserve, covers 24 000 square kilometres – increasing still further if we include the contiguous areas of Lake Manyara and Tarangire national parks. Yet, the Serengeti ecosystem has several orders of magnitude more antelope than Kruger; there are more than 1.4 million migratory blue wildebeest alone in the Serengeti (figures 8.6a–b), but only around 14 000 in Kruger. The soils are more fertile and lion densities higher in the Serengeti than in Kruger, but these differences are not sufficient to account for this enormous difference. Recent work by Norman Owen-Smith (2006) suggests that it is the denser vegetation of Kruger that creates a ‘landscape of fear’ for wildebeest, which choose to remain in relatively small open grassland patches among the vast woodlands and thickets that predominate, presumably to avoid predation by lions, their main predator. The Serengeti, by contrast, is mostly open grasslands, which allow wildebeest to spot lions a long distance off. Owen-Smith suggests that if we were to compare the extent of these grassland patches in the two areas, we would find that this would tally with the numbers of wildebeest. Another way of expressing this is that Kruger is not ideal wildebeest habitat. Wildebeest populations have been counted regularly in both parks for decades, since the 1960s in the Serengeti and the 1970s in Kruger (Owen-Smith 2006). In Kruger, wildebeest populations fluctuate roughly between 10 000 and 14 000 individuals (Gandiwa et al. 2016). In contrast, the Serengeti population started out at a low of around 200 000 individuals in 1960, increasing to 187

(a)

(b) Figure 8.6. a–b. Blue wildebeest (Connochaetes gnou) in the Maasai Mara National Reserve, Kenya. Photographs by Ara Monadjem.

Fluctuating Populations

a peak of 1.4 million in 1978 and then fluctuating slightly below this figure up to the 1993–1994 drought, and declining further since then (Mduma et al. 1999; Ogutu et al. 2011). In the Serengeti, wildebeest populations are regulated by food, which in turn is affected by rainfall, and drought years can hit the population hard. For example, almost 20 per cent of the population perished in the 1993–1994 drought. But compared with buffalo populations, this is rather mild. During the same period the buffalo population in the Maasai Mara National Reserve, which abuts the Serengeti National Park to the north, and in surrounding pastoral ranches, crashed from about 13 000 to 3 000 individuals within a matter of a few months, representing a four-fold reduction (Dublin and Ogutu 2015). The interesting point about both these populations is that the declines were density-dependent. In the wildebeest population, density dependence was most evident as an increase in the mortality of adults. Juvenile mortality was only marginally density-dependent, which demonstrated that other factors, not related to population size, were probably more important in this age class. Predation, mostly by lions, played a smaller role than food supply in controlling the wildebeest population, indicating that this population is regulated ‘bottom up’ and not ‘top down’.5 Density-dependent regulation, of course, implies that intra-species competition – that is, competition between members of the same species – will be great. This is because the population of that species is typically at or near its carrying capacity and therefore individuals in the population will have to compete for food. It may be difficult for us to comprehend how wildebeest food, essentially grass, can be in short supply except in the grip of the worst drought. Gazing out onto a grassy plain, we imagine limitless quantities of grass being available. But not all grass is equal. Some grass species are more nutritious to antelopes than other species, and some grass parts – during some seasons – are more nutritious than other parts. So, population fluctuations in antelopes do occur and are typically mediated by rainfall and predation. We have seen that population fluctuations in r-selected species can be extreme. We have now also seen that even populations of K-selected species undergo changes, albeit far less dramatic ones than in r-selected species. Norman Owen-Smith and Gus Mills plotted the population trajectories of 12 species of large ungulate in the Kruger National Park over two decades, from the mid-1970s to the mid-1990s (Owen-Smith and Mills 2006). The giraffe (Giraffa camelopardalis) population was perhaps the most stable over this period, 189

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but even here they recorded a twofold difference between the highest and lowest numbers. Some species declined, with four in particular reaching virtual extinction and being saved only by direct intervention from wildlife managers. These four are sable (Hippotragus niger), roan antelope (Hippotragus equinus), tsessebe (Damaliscus lunatus) and eland (Taurotragus oryx), and they have caused considerable concern to managers and conservationists alike. If we are unable to maintain sustainable populations of these species in a park the size of Kruger, what chance do we have of protecting them anywhere in Africa? The reason for their decline is not fully understood, but appears to be connected to two possibly interrelated factors: an extended period of low rainfall starting in the 1980s; and the construction of additional artificial watering points away from rivers and existing water bodies. The latter has had the effect of drawing wildebeest and zebra,

Indian Ocean Atlantic Ocean

0

500

1000km

Figure 8.7. The roan antelope (Hippotragus equinus) occupies a wide distribution across the African continent (grey shading). However, population sizes (and hence densities) are not uniform across this distribution, with certain regions supporting far larger populations than others. The known populations that harbour 1 000 or more individuals are shown as black circles; note the greater preponderance of large populations in west Africa. Sources: The map is based on the IUCN (2019) distribution map for roan; the location of large populations is taken from Havemann et al. (2016).

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which typically need to drink daily, deeper into the park and away from perennial sources of water (typically the larger rivers that meander through Kruger). Following closely on the heels of the wildebeest and zebra populations were lions, which were the proximate cause of the decline of the four rare antelope species. This finally brings us to the main point of this chapter. When we think of the distribution of a species we tend to think in terms of uniform population densities across the space it occupies. Looking at a field guide, for example, we do not normally imagine significant variations in population density across the coloured area indicating ‘resident’ on the distribution map. Yet, this is far more likely to be the case than a population with a uniformly dense distribution. Take a look at the distribution of the roan antelope shown on the map in figure 8.7. This species occurs widely across the savannas of Africa. But this map is highly, albeit unintentionally, misleading. If, instead, we plot a map showing the largest populations of roan with more than a thousand individuals (the dots in figure 8.7), we see that in fact roan is mostly restricted to the northern Guinean savannas. We now see that the population of this antelope is anything but uniform. We would discern the same pattern for any species we choose to examine in this way. Therefore, ecologists and conservationists need to consider population density, which requires an understanding of the factors that influence the population. *** In this chapter, we have examined the role played by population density in the ecology of African mammals. Mammalian populations are typically not uniformly distributed across a landscape or over time, with population fluctuations being the norm for all species. The magnitude of these fluctuations differs radically, depending on the life history of the species. One life history strategy – that of the so-called r-selected species – is to maximise productivity by creating lots of offspring at the expense of individual survival. The other strategy – that of the so-called K-selected species – is to maximise efficiency in resource use by investing in raising fewer, more competitive offspring, while better safeguarding individual survival. These two contrasting strategies define the population growth capacity of different species, with the former thriving in unpredictable or variable environments, and the latter doing well in more stable situations. The two strategies generate distinctly different population dynamics. Furthermore, populations are regulated by bottom-up (food supply) or top-down (predation, disease) factors. In the next chapter, we will look at how humans fit into this ecological picture. 191

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or much of this book we have discussed life on Earth as if humans were not part of it. This somewhat bizarre attitude is relatively common among ecologists, whose aim is to study animals in their natural habitats. We humans typically assume that ‘natural’ does not encompass our own presence and influence – perhaps because we find it easier to consider the natural world as something separate from the complexities of our own lives. This way of thinking is most obvious when we discuss conservation issues (see chapter 10). However, not only is it scientifically flawed to remove humans from studies of the ‘natural’ environment, but also many of the ‘natural’ habitats that we observe today are actually anthropogenic; in other words, they were created by humans. In fact, we have now entered a new epoch in the geological history of the Earth, the Anthropocene, in which humans are directly impacting planet-defining processes such as the carbon and nitrogen cycles. To consider any part of the Earth, even remote uninhabited islands, as divorced from humanity is thus simply untenable. Although we have only recently entered the Anthropocene, humans have been around for several million years and have been interacting with other mammals, particularly in Africa, since the dawn of our existence. In this chapter, we will start by examining the nature of these interactions, then look at ways in which we can benefit from the various ecosystem services that other mammals, and in particular small mammals, provide.

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THE ANTHROPOCENE Geologists have divided the history of the Earth into discrete periods of time, each typically spanning tens of millions of years, and most of them probably unheard of by the layperson – although a few, such as the Jurassic, have made it into popular culture. The Jurassic Period ran from about 201 to 152 million years ago and was one of three periods dominated by dinosaurs. These periods are not equal in length, like the 60-minute period that divides the day into hours.1 Instead, geological periods are punctuated by massive events with global consequences that are clearly observable in the stratigraphic record, including in rocks, ice cores and marine sediments. For example, the break between the Cretaceous and Palaeocene (66 million years ago), which saw the demise of the dinosaurs and the rise of the mammals (see chapter 3), was marked by the impact of a large meteorite, which left a band of iridium – a chemical element found in much greater abundance in meteorites than within the Earth’s crust – in rocks of that age, which geologists have discovered in numerous rocks of the same age around the world. Traditionally, our present age is referred to as the Holocene epoch (see table 3.1).2 However, good arguments and evidence have been put forward to show that recent human activity has indeed had a significant enough global impact to have left a mark in the stratigraphic record (Lewis and Maslin 2015). According to some geologists (and as argued in this chapter), we have now transited from the Holocene to the Anthropocene epoch. It is well known, of course, that levels of atmospheric carbon dioxide (CO2) are the highest they have been in millions of years. Perhaps less well known is that we have altered the nitrogen cycle even more severely, through the manufacturing of artificial fertilisers. Indeed, we have to look back 2.5 billion years for a natural comparison (Lewis and Maslin 2015). The endings of five of those geological periods are defined by the mass extinction of species.3 The most devastating of these mass extinctions was the end-Permian event, in which perhaps 90 per cent of all species on Earth were obliterated, but the end-Cretaceous event is probably the best known as it was responsible for the demise of the dinosaurs. Today we are witnessing the sixth mass extinction. The culprit is not a meteorite or some super-volcano, but human activity. This too will be visible in the geological record, and perhaps will be discovered by an intelligent species present on Earth in a few million years’ time. So, what does the Anthropocene look like? In particular, what sort of relationship do we humans have with the other mammals with which we share this 193

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Figure 9.1. A herd of sheep feeding in a conservancy adjacent to the Maasai Mara National Game Reserve, Kenya, where they compete with wild herbivores for grazing. Photograph by Ara Monadjem.

planet? Of course, we have killed so many of the larger, more menacing ones that, sadly, most of these remain only in our myths and legends. Wolves, tigers and, increasingly, lions, have effectively been wiped out everywhere except in places in which we wish them to persist, such as national parks and other protected areas.4 Likewise, large migratory herds of ungulates, which would have been a normal component of most ecosystems, today persist only in the remotest corners of the Earth, or have been transformed, via domestication, into livestock (figure 9.1). Furthermore, many of the large, non-human mammals that have managed to persist now find themselves in a state of perpetual friction with humans, which has been dubbed ‘human-wildlife conflict’.

HUMANS AND SMALL MAMMALS: THE NEGATIVES I do not particularly like the term ‘human-wildlife conflict’. It suggests that wildlife is going out of its way to do us harm. In reality, the motivation behind 194

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the ‘conflict’ is very much one-sided. It is we humans that are in conflict with wildlife, and not the other way around. In fact, I doubt whether any wildlife species even understands the concept of conflict. An elephant that destroys a maize field only sees a patch of nutritious food. Of course, there is no doubt that the impact of some mammals on human livelihoods can be severe and will need to be addressed if we wish the two to coexist (figure 9.2). However, while the impact of large mammals such as elephants on human livelihoods has been relatively well studied, we still understand very little about how small mammals affect us. We know that they eat our crops and give us diseases, but these are general, sweeping statements. Exactly how much of our crops do they eat? Do they eat all crops equally? What diseases do they ‘give’ us and how are these diseases transmitted? And, in any case, who exactly are ‘they’? Although rats and mice have been viewed as pests across the world for millennia, their precise impacts on humans have not always been quantified or even clearly understood. Despite tens of millions of people dying of plague, known in medieval Europe as the ‘Black Death’, the link between the bacterium responsible for the disease (Yersinia pestis) and fleas and rats was not

Figure 9.2. A farmer building a chilli fence to keep elephants out of his fields, Luangwa Valley, Zambia. Photograph by Mike Unwin.

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established until the 1890s, by which time plague had all but vanished from the region. Interestingly, recent studies by Nils Stenseth’s lab in Oslo, Norway, have shown that plague outbreaks in Europe during this period were driven by reintroductions from rodent reservoirs in central Asia, and most probably carried by caravans plying the Silk Road trade route (Schmid et al. 2015).5 There is no evidence that plague persisted in populations of the black rat resident in Europe during this time, destroying the myth that these rats served as reservoirs of this deadly disease. Our knowledge of African rodent pests is even more limited. We do know that rodents destroy crops in Africa (Fiedler 1988; Makundi et al. 1999), but the scale of this destruction is not well known – or at least was not, until relatively recently. Only a few studies have been conducted in this field, partly because conventional wisdom dictated that crop damage by rats and mice was negligible compared with that wrought by other threats such as drought and insects, and partly because of a general apathy towards things that we cannot readily control. However, we have been proved wrong on both counts: rodents may have severe impacts on crops; and yet we can do something about it (Swanepoel et al. 2017). My entry into the field of applied ecology Before I go into further detail, let me relate how I got involved in this field in the first place. I started my career at the University of Swaziland (now the University of Eswatini) shortly after my long-term colleague and friend Themb’a Mahlaba started his, both of us in the same Department of Biological Sciences. I clearly remember, in the late 1990s, Mahlaba suggesting that we make our research more applied, particularly to investigate small mammals in agricultural settings. I also clearly remember my response to him: ‘No thanks!’ I only wanted to study animals in their ‘natural’ habitats and couldn’t think of anything worse than trapping rodents in maize fields. Working in such environments takes the fun out of studying wild animals, mostly because so few species persist in agricultural landscapes. What chance do you have of seeing an antelope, let alone an elephant or a rhino, in a maize field? However, as humanity has increased its agricultural production in recent decades, the amount of land under farming of one kind or another has also increased (figure 9.3). Now, these farms do not just hold important 196

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Figure 9.3. A typical homestead with an agricultural field in the foreground, Eswatini. Photograph by Ara Monadjem.

populations of native species: they also form the very matrix within which protected areas are inserted. Protected areas in isolation will not retain their biodiversity for long, which is why connecting them via ‘corridors’ to form a network of protected areas has been the focus of conservationists during the past decade. With this changed perspective, farmland suddenly is no longer simply a biodiversity-poor ecosystem: it is the fundamental system that links everything together. Understanding ecological processes in agricultural landscapes, therefore, is of primary importance to ultimately conserving our biodiversity. This simple line of logic did not come to me quickly or easily. In fact, over the next ten years, Mahlaba kept on repeating his conviction that we should work in agricultural areas, and I skilfully kept on evading it. That is, until I met Steve Belmain from the Natural Resources Institute at the University of Greenwich, UK, at a rodent management conference held in Hanoi, Vietnam in 2006. Belmain’s presentation was excellent. He manoeuvred nimbly between the disciplines of science and social science to explain the importance of interdisciplinary research in managing Africa’s pest rodents. Belmain 197

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was already a world authority on the management of pest species in agricultural landscapes, so when he asked whether I would be interested in joining an international project looking at ecologically sensitive ways of controlling pest rodents, I could hardly say no. The project, under his leadership and involving researchers from South Africa, Namibia, Tanzania and Eswatini, was dubbed ECORAT.6 Its focus was on developing ecologically based pest rodent management specifically for small-scale (subsistence) agriculture in Africa. In other words, ECORAT aimed to assist the poorest farmers on the continent. The work was challenging because, for the first time in my research career, I was confronted with a human element. I did not particularly relish this new challenge and left most of the ‘social research’ to Mahlaba, who thrives in human-dominated landscapes – whereas I am best left to work with animals and as far away from people as possible.7 Although I was not convinced of it at the time, our work did actually have an impact. First, we quantified the scale of the rodent pest problem and demonstrated that it was big enough to warrant further attention. Second, we confirmed that rats and mice can damage crops and affect yields in the fields (‘pre-harvest losses’), as well as during storage (‘post-harvest losses’). By way of example, we demonstrated that farmers who stored their maize harvests in traditional open cribs, usually woven of grass (figure 9.4), experienced far higher losses than those who stored them in closed cribs or sacks due to the consumption of grain by rats and/or the contamination of the remaining grain with the rodents’ faeces, urine and hair. The numbers we recorded were sobering: grain in open cribs was damaged or contaminated by rats at a rate of 40 per cent per month (Mdangi et al. 2013). Despite its magnitude, this damage is not easily observed because the contaminants are relatively small – as is the damage to individual grains, which may be no more than a single gnaw mark. This may explain why small-scale farmers had not noticed the scale of their post-harvest losses before. Either way, it amounts to significant losses, both in terms of the sheer mass of wasted grain and the indirect effects of illness caused by rodent contaminants. These losses are especially significant when added to pre-harvest losses, which can amount to more than 90 per cent of the yield in extremely bad years, although they are generally around 5 to 10 per cent per annum in east Africa (Makundi et al. 1999).

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Figure 9.4. A traditional storage structure for holding harvested maize in Tanzania, with Steve Belmain (right) from the University of Greenwich, UK, who has spearheaded much of the research that I have been involved with pertaining to small-scale farmers and rodents. Nomfundo Dlamini (left) was the ECORAT manager in 2007–2008. Photograph by Ara Monadjem.

Working with farming communities Small-scale farmers in Africa seldom have access to finance, so any technologies developed for them must necessarily be cheap and readily accessible. Through the ECORAT project, which ran from 2007 to 2009, and subsequently the StopRats (2014–2016) and EcoRodMan (2018–2021) projects, we attempted to develop solutions that these farmers could easily adopt without requiring additional funding for equipment or training. We also needed to ensure that any equipment required should not be labour-intensive, or it might simply not be

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used. But we also had other considerations, notably the impact on the environment. We wanted to devise ways of dealing with rodent pests that would not harm non-target species or poison the environment, hence our philosophy of ‘ecologically based pest rodent management’. We started out with a simple experiment to test whether community trapping by farmers could control populations of pest rodents. We did this by identifying villages, located in the participating countries mentioned earlier, that were willing to participate, and then randomly grouping them into those that would trap rats – using cheap, commercially available kill-traps – in their homes and fields, and those that would not.8 In each of the three countries (Eswatini, Tanzania and Namibia), we set up two intervention communities where trapping took place and two control communities where it did not. Intervention communities were given 100 kill-traps (valued at about US$50 in total) that were set nightly for a year, rotating through the community so that each homestead set two traps for a week per month. With this relatively minimal individual effort, the intervention communities were able to greatly reduce the rodent population in their areas in comparison with the control communities (Taylor, Downs et al. 2012). Furthermore, damage to stored grain was also reduced. All this with just two traps shared between four households! We also tested a variety of cheap alternatives for storing harvested grain that appeared to reduce losses by an enormous margin compared with traditional bags. Hermetic bags reduce the levels of oxygen and increase levels of carbon dioxide, making the bags unsuitable for any insect pests trapped inside with the stored grain (Mlambo et al. 2017). In addition, such bags also reduce leakage of scent from the stored grain within the bag, making it more difficult for rodents outside the bag to detect the stored grain. Like community trapping, the introduction of hermetic bags is another cheap and cost-effective way for subsistence farmers to reduce grain losses (Alemu et al. 2021), which in this case are post-harvest losses. But our work in farming communities was not only about ‘managing’ (put more bluntly, ‘killing’) pests, which of course was welcomed by these communities: we also wanted to make a positive contribution to biodiversity conservation in these heavily transformed landscapes. There are many potential ways in which we could have attempted to achieve this. For example, we could have attempted to draft new laws strictly prohibiting the destruction of species and ecosystems within the farmlands in question. This would not have been a feasible option, so we opted for an alternative. We set out to demonstrate the 200

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positive role that small mammals play in agricultural landscapes as providers of essential ecosystem services. If farmers came to view these creatures as beneficial, we reasoned, then they may want to conserve them in order to reduce their costs and/or increase their yields. We thus needed to investigate how biodiversity might benefit farmers, especially with regard to small mammals.

HUMANS AND SMALL MAMMALS: THE POSITIVES It is generally easier to appreciate how wild animals ruin farming operations than how they might assist them. A single elephant can trample and destroy an entire family’s staple crop in one night. A large predator such as a lion can kill a cow or goat in a matter of seconds. An infestation of mice can nibble away at maize or rice plants, causing serious damage. This is not to mention all the possible diseases that such mammals might transmit to either humans or livestock. However, wild mammals also provide numerous benefits to farmers, and humanity in general, which are far less known or appreciated (Lacher et al. 2019). These benefits are known as ecological or ecosystem services; I  have already discussed them in chapters 1 and 6. In a broad-brush approach, table 9.1 lists the ecological services provided by African mammals. The list is a lengthy one, but it does not immediately reveal what these services look like in reality. To get a better understanding of this subject, therefore, I will give a few examples, drawn mostly from work in which I have been personally involved. This will allow us to delve deeper into the rich tapestry of interactions that constitutes the natural world. Ecosystem services provided by rodents Earlier, I painted a negative picture of rodents by describing their interactions with African small-scale farmers. Yet only a small fraction of African rodents are harmful to humans. A recent review of the topic listed just 10 genera implicated as pests (Swanepoel et al. 2017), from the 89 genera known to occur in sub-Saharan Africa (Monadjem, Taylor et al. 2015); perhaps a dozen species are responsible for most of this damage. With around 500 species of rodent recorded from the continent, you can easily grasp how unrepresentative this

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Table 9.1. Examples of ecosystem services provided by African mammals. Service

Examples

Herbivory

Grazing lawns created by white rhinoceroses are often completely different in species composition and structure from surrounding habitats, creating landscape heterogeneity.

Nutrient cycling

Nutrients are injected into wetland systems by grazing hippopotamuses that feed on land but spend the day in water.

Seed dispersal

Granivorous rodents cache seeds underground and hence provide a safe environment in which many seeds can germinate.

Pollination

Rodents in the fynbos biome of South Africa have been shown to pollinate flowering plants.

Soil aeration

Mole-rats and golden moles create burrows and chambers underground that assist in aerating the soil and increasing rainwater infiltration.

Carcass removal

Many mammalian carnivores scavenge, which helps to remove carcasses of large ungulates, thus controlling fly populations that use these carcasses as breeding grounds.

Prey

Terrestrial small mammals form the main prey for many groups of predators, including snakes, hawks, owls and small and medium-sized mammalian carnivores such as genets, mongooses, servals and jackals.

Ecosystem engineering

Aardvarks dig burrows that are subsequently used by dozens of other vertebrate species and countless invertebrates that are not able to create these shelters themselves.

Predation

Small and medium-sized carnivorous mammals can assist in reducing populations of pest rodents, which may be especially important in agricultural settings.

is. By far the majority of rodent species do us no harm at all, and many scores of species – or more – actually provide us with benefits. Some of these benefits are obvious and well known, such as rodents forming the prey base for higher trophic levels, particularly as food for snakes, mesocarnivores and birds of prey. But others are intriguingly obscure and poorly known: for example, rodents pollinate flowering plants in the fynbos and succulent Karoo biomes of South Africa. Another example of the beneficial roles played by rodents comes from a study that we recently conducted in Eswatini to test whether rats and mice could potentially assist with checking bush encroachment (as discussed in chapter 6). We know that some rodents, such as members of the genus Saccostomus (pouched mice), are granivorous, feeding on seeds. Such species, of course, destroy any seeds that they consume, but may inadvertently also contribute 202

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to the success of the plants whose seeds they eat by caching some of these seeds in their underground burrow system. Some of these stored seeds may be consumed at a later time by the rodent, but many escape to germinate in  relative safety from other seed predators. Seeds are also consumed, often in large quantities, by species that are more flexible in their diet, also taking green plant matter and insects, depending on the season and their availability. Such species include members of the genus Lemniscomys (striped mice). These beautiful but nervous mice are typically light brown in colour, with one or more conspicuous black lines (depending on the species) running down their back. The species that occurs throughout much of southern African is Lemniscomys rosalia, which feeds predominantly on green plant matter but also takes seeds (figure 9.5). Unlike Saccostomus, Lemniscomys does not cache these seeds and can therefore be viewed as a seed predator. In a simple experiment, we loaded trays with the seeds of two common savanna tree species found in Eswatini and elsewhere in the region, and placed them under tufts of grass on the ground. One of these species, Dichrostachys cinerea, is a notorious invader and the main contributor to bush encroachment in our area, while

Figure 9.5. A single-striped grass mouse (Lemniscomys rosalia) visiting a feeding station, Eswatini. Photograph by Annie Loggins.

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the other one is a largish tree, Senegalia nigrescens, that does not contribute to bush encroachment. We demonstrated that rodent seed predators preferred the small seeds of the encroacher, and importantly, we showed that their activity was severely curtailed in areas without adequate grass cover (Teman et al. 2021). Lemniscomys rosalia, like many savanna rodents, relies on good grass cover, which presumably allows it to avoid being detected and captured by a hungry serval, black-shouldered kite, or other predator. Hence, rodents such as Lemniscomys rosalia could potentially be important allies in our fight against bush encroachment, provided that we allow them the grass cover in which to operate. Recently, researchers from around the world have demonstrated the impressive ecosystem services provided by bats (Jones et al. 2009). I discussed these in chapter 1; here I want to highlight the fact that bats potentially save farmers in the USA at least US$3 billion annually that would be spent on pesticides and other activities to reduce the crop damage caused by insects, were the bats not there (Boyles et al. 2011). Until very recently, we did not have comparable figures for Africa, but Peter Taylor’s efforts in Venda, Limpopo Province, in northern South Africa, have quantified the ecosystem services provided by bats in macadamia orchards. To do this, Taylor’s PhD student Valerie Linden devised a clever and demanding experiment that involved setting up 48 cages around macadamia trees to exclude diurnal and nocturnal vertebrates, birds and bats respectively. Birds and bats are the main predators of macadamia pests, which include the notorious Nezara stinkbug (figure 9.6) (Weier et al. 2019). By excluding these predators, Linden and her team were thus able to quantify the damage caused by the pest insects. When both birds and bats were excluded, crop yields plummeted by 60 per cent, causing financial losses of roughly US$5 000 per hectare per year (Linden et al. 2019), with birds contributing slightly more than bats to the savings that farmers were making. Such losses are significant and clearly signal the economic value of having bats and birds around. Of course, we must remember that any such savings for the farmer would not take the form of dollars in the pocket – especially for subsistence farmers who, by definition, do not earn any money from their farming operations, and generally are unable to pay for insecticides or other inputs. The ‘losses’ these farmers experience are decreases in yields, as insects and other pests take their toll. Since many subsistence farmers are living hand-to-mouth, any reduction 204

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Figure 9.6. An Egyptian slit-faced bat (Nycteris thebaica), feeding on a stinkbug (Nezara), which is a pest of macadamia trees. Photograph © MerlinTuttle.org.

in yield is potentially the difference between survival and starvation. The losses we are talking about here are thus far more severe than those measurable by financial hardship alone. Mammals that control pest rodents During the StopRats project I referred to above, we also investigated the role of mammalian predators in controlling the populations of pest rodents, particularly rats and mice. Although we had already demonstrated that pest rodents could be controlled using break-back traps, it would be far more satisfying if we could show that predators do this work naturally. Hence, we dedicated an entire study to understanding the relationship between rats and their predators. These predators included domestic cats, domestic dogs, and 205

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Figure 9.7. Lourens Swanepoel fitting a yellow mongoose (Cynictis penicillata) with a tracking device (right). Photograph by Wayne Matthews.

native or wild mammalian predators such as servals, mongooses and genets. We also considered the role of owls (Labuschagne et al. 2016). This research into predator-prey interactions was ably coordinated by Lourens Swanepoel from the University of Venda, South Africa (figure 9.7). Swanepoel possesses a sharp mind and an insatiable interest in – and impressive knowledge of – carnivorous mammals. Working with two relatively poor farming communities in the Limpopo province of northern South Africa, he and his team were able to map out the predatory landscape in and around these communities by setting dozens of cameras traps that recorded the local predators.9 The list they amassed was impressively long, and included such species as Meller’s mongoose (Rhynchogale melleri, figure 9.8) that are very rarely seen (Williams et al. 2017). This ingenious study did not only identify predators but was also able to observe where in the landscape each species foraged. In the villages, the predators turned out to be largely dogs and cats that patrolled the territory, with the occasional incursion from something wilder. In the fields, however, these domestic predators gave way to native species, such as mongooses and 206

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Figure 9.8. A Meller’s mongoose (Rhynchogale melleri ) with three young in agricultural fields in Venda, northern South Africa. Photogaph by Lourens Swanepoel.

genets. It was thus clear that predators had partitioned the landscape – with domestic predators holding sway in human habitation, and native mammals in the fields and surrounding bush. It was encouraging, also, to see that such a diverse native mammalian predator community was still present in farmland. The next step in this study was to investigate any correlation between the presence and whereabouts of these predators and the abundance and activity of pest rodents. Unfortunately, as often happens in ecological studies, a natural phenomenon occurred that made the study all but impossible. Southern Africa was gripped by a severe drought in the summer of 2015–2016, which decimated rodent populations throughout the region. During follow-up rodent surveys, Swanepoel’s team was only able to capture two individual rats. This is way too small a sample to allow for any meaningful ecological analysis. Although the drought also affected Eswatini – and was the worst there in living memory – the rats did not completely disappear, and so our StopRats team was able to address this aspect of the study. While Swanepoel’s team was mapping mammalian carnivores in Venda, the Emaswati team, coordinated by Themb’a 207

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Mahlaba and myself, was mapping rat activity in and around homesteads in three different rural communities in Eswatini. Our rat community here is dominated by the introduced black rat (Rattus rattus), also known as the roof, house, or ship rat. This amazingly adaptable animal originally evolved in South East Asia, but has been transported across the world by humans and, throughout its range, is associated with human habitation, living in the roofs of houses or simply inside the house itself. It is a relatively large and aggressive rodent, easily displacing native species from its anthropogenic habitat (Monadjem et al. 2011), although the even larger brown rat (Rattus norvegicus) tends to displace it where their distributions overlap.10 In Eswatini, as in much of Africa, the black rat is an unwelcome but ever-present guest in the homes of both rich and poor, where its tireless gnawing can cause substantial damage to both infrastructure (including electric wires that it chews) and human body parts (mostly while the person is asleep in bed), not to mention its depredation of grain stores. This is a pest that causes much grief to the rich but even more to the poor. Our aim in mapping its activity was to try to understand its relationship with domestic dogs and cats. In particular, we wanted to know whether the presence of these domesticated predators affected its activity patterns. The domestic cat is descended from the African wildcat (Felis lybica) and was first domesticated in ancient Egypt, where no doubt it served to control rats that feasted on stored grain. We thus hypothesised that we would detect reduced rat activity in homesteads with cats but that dogs would not have any real impact. How wrong we were! Rat activity at homes with dogs but no cats was no different to that in homes with neither dogs nor cats. This finding did not surprise us. However, homes with only cats (that is, no dogs) also showed similarly high rat activity, comparable to homes without any pets. It was only when we examined rat activity at homes with both dogs and cats that we found a significant difference: rats were far less active in these homes (Mahlaba et al. 2017). Our simple, low-tech method for measuring rat activity required ordinary white bath tiles and a kerosene lamp. Each tile was held over the flame of the kerosene lamp until it was sooted over so that it turned completely black. We then placed these tiles at strategic positions within the home where we expected rat activity, such as along walls in the kitchen or in the storeroom. The tiles were inspected each morning for rat footprints, which show up clearly in the soot. These footprints were counted and used to represent an index of rat activity: the more footprints on a tile, the more activity we could infer for that homestead. 208

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Our study revealed a clear – and highly surprising – pattern, in which households with both cats and dogs had significantly lower rat activity. This pattern was consistent across different communities, tens of kilometres apart, and in different seasons. At first it appeared difficult to interpret, and perhaps even counter-intuitive. Surely cats are better hunters of rats than dogs? Why would a rat worry about a dog, which does not have a cat’s specialised expertise in hunting small mammals? We do not know the answer to this question, but we have proposed the following as an explanation, one that still needs to be tested. A rat confronted with a cat, or the scent of a cat, would react in a particular way in order to reduce its chances of falling victim – perhaps taking evasive action by bolting down the nearest hole. A rat confronted with a dog, however, behaves in a different way – perhaps by climbing up and out of the way, ‘knowing’ that a dog might be able to dig it out of a burrow but cannot climb or leap like a cat. However, when a rat is confronted by both a cat and a dog, or their scents, in places where both those predators occur side by side, it may experience conflicting sensations, causing it sufficient confusion or fear to suppress its evasive activity – and perhaps even drive it outside. We tried to test this hypothesis by conducting what we thought would be a relatively simple experiment. Our design was to introduce dog and/or cat faeces randomly into houses without cats or dogs, and see whether the introduction of predator scent would affect rat activity. Unfortunately, as simple as this may sound, the home owners in question were understandably less than keen to have us soil their living space with excrement. Thus our original experiment did not work out, and we are still trying to devise ways of testing our hypothesis without inconveniencing the people whose houses have become our study sites. Experienced zoologists and ecologists will immediately see that I have oversimplified matters in this section. There is far more to human-animal conflict than rats and cats in farmers’ homes. And ecosystem services are far more diverse than merely bats feeding on pest insects over agricultural fields. I chose these examples because I have had first-hand experience with them and wanted to offer a ‘behind the scenes’ look at how researchers are addressing this matter. They form case studies that offer insight into a broad subject by examining one or two aspects of it in greater detail. In an attempt to show some of the greater complexity involved, I will end this chapter by looking at the thorny issue of disease. 209

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SMALL MAMMALS AND DISEASES Virologists love small mammals. This is because bats and rodents provide the hosts for many of the diseases currently afflicting humanity, and for the ‘emerging infectious diseases’ that are thought likely to be the diseases of the future (Han et al. 2016). This, though, may be an unfair conclusion. Bats and rodents are super-diverse members of the class Mammalia (see chapter 1) and, purely on this basis, one may predict that they have a greater number of diseases associated with them. In fact, a recent study has shown that bats and rodents have proportionately the same number of diseases per species as other groups of mammals (Mollentze and Streicker 2020). This, however, does not change the fact that in absolute terms, bats and rodents still support a large number of diseases. It may be the reason why Wanda Markotter (figure 9.9), one of Africa’s top virologists specialising in bat diseases, loves bats: they provide her with abundant samples of viruses and bacteria on which she and her large group of students, postdocs and collaborators can get to work. To be fair, she also loves bats for their own sake, as cute and interesting creatures with amazing habits. In her recent review of bat-borne viruses in Africa, Markotter and her co-authors list potential zoonotic diseases as most probable in four viral families: Coronaviridae, Filoviridae, Paramyxoviridae and Rhabdoviridae (Markotter et al. 2020).11 A zoonosis is an infectious disease carried by an animal that can be naturally transmitted to humans. Well-known examples include rabies, Ebola, bird flu and bubonic plague, all of which proliferate in Africa, while less familiar – though equally unwelcome – examples are leptospirosis, Lassa fever and the Middle East Respiratory Syndrome (commonly known as MERS). Since early 2020, all of these have been eclipsed, at least in the public consciousness, by COVID-19. This latest virus – now a major global pandemic that has killed millions of people worldwide and fundamentally affected all sectors of human society – is also thought to be a zoonotic disease. I will not provide an overview of zoonotic diseases here, but instead have chosen a few examples to illustrate the role of the four viral families mentioned above. The first thing to note, however, is that we do not know all that much about zoonoses, despite the fact that governments and international funding agencies are putting millions of dollars into the study of infectious diseases. There are numerous major institutions, including the World Health Organisation and the 210

(a)

(b) Figure 9.9. (a) Wanda Markotter (left) dressed in protective gear while extracting viruses from living bats, and Marinda Mortlock (right), a post-doctoral researcher in Markotter’s lab, assisting with the process; the bats were released unharmed after they were sampled. (b) Wanda Markotter removing her mask after a hard morning of sampling. Photographs by Ara Monadjem.

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US Centers for Disease Control and Prevention, which not only deal with combating such diseases but also emphasise the importance of understanding their ‘ecology’ and of diagnosing new diseases. With so much research muscle behind the subject, one might expect that we would know all, or at least most, of what we need to know about it. Sadly, this is far from the case. Not only are we still in the dark about the basic biology of many of the nastiest diseases known to us, but we are also still discovering new zoonotic diseases all the time. To give one well-known example, the Ebola virus (a member of the Filoviridae) epidemic of 2013–2016 is recorded as having killed more than 11 000 people in west Africa – a figure that is almost certainly an underestimate. Fortunately, the epidemic was brought under control before it could spread globally and cause even more human misery, on the scale of the COVID-19 pandemic. Yet we still do not know the host species for Ebola, though we have been searching for decades. Where does the disease ‘hide’ between outbreaks? Is it in bats, as in the closely related Marburg’s virus (also a Filoviridae), whose host is the Egyptian fruit bat (Rousettus aegyptiacus) (Amman et al. 2015)? Certainly, the Ebola virus has been detected in many different species of bat, but this does not confirm that they are the hosts. For a species to be a host we must demonstrate two things: first, that it does not get sick from the disease – or at least it recovers instead of dying; and second, that it can shed the virus through, for example, faeces or urine. The disease itself is relatively new – or, more correctly, scientists have not known about it for very long, with the first suspected outbreak being from the Ebola River region in the Democratic Republic of the Congo (then Zaire), in 1976. Other zoonoses have been discovered even more recently. MERS (Coronaviridae) was first reported in humans in 2012, in Jordan and Saudi Arabia. Like Ebola, MERS is a nasty disease that kills up to four in every ten patients. The host of MERS appears to be camels, but the disease probably originated in bats. However, the origins of this virus are still not understood. And, of course, there is SARS-CoV-2 (also Coronaviridae), better known as COVID-19. At the time of writing, in August 2022, this devastating pandemic has claimed more than 6.49 million victims worldwide (almost certainly ­under-reported) and the death toll continues to rise. Besides the immediate human suffering it has caused, the social and economic damage – including national ‘lockdown’ programmes and a halt to international travel and trade – has been incalculable. While some parts of the world are now rolling out vaccine 212

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programmes, other regions are seeing a surge in infections and a proliferation of variant strains. This book is not the place to investigate the causes and impact of this crisis – a subject that currently monopolises global thinking across all sectors and receives exhaustive coverage elsewhere. Nonetheless, it is worth reminding ourselves that the COVID-19 virus is simply the latest in a long history of zoonotic diseases; current thinking holds that it was first transmitted to humans in China and/or South East Asia via bats or via wild animals held captive in illegal ‘wet-food’ markets – and that there will be many more such diseases to follow. This current crisis may be a long-overdue rallying call to treat zoonoses more seriously. In contrast, diseases caused by viruses of the families Paramyxoviridae and Rhabdoviridae appear to have had less impact on humans in Africa. Hendra and Nipah viruses are two species of Henipavirus (Paramyxoviridae) that first appeared in Australia (in horses) and Asia (in pigs), respectively, with mortality rates in humans being as high as 50 per cent or more, and with survivors frequently having long-term disabilities.12 It is, therefore, rather worrying that henipaviruses have now been isolated from several species of fruit bat across much of Africa.13 In the review paper I referred to above, Markotter and her coauthors call for increased surveillance of bats for henipaviruses. The remain­ing family of viruses listed in that review is the Rhabdoviridae. This includes the dreaded rabies, closely associated with dogs and other carnivores, for which – without vaccination – the mortality rate in humans is effectively 100 per cent.14 Rabies is one of about 16 described species in the genus Lyssavirus – although this number keeps rising as new ones are discovered – which in Africa is closely associated with dogs and other carnivores. The other species are referred to as rabies-related lyssaviruses, of which three African species are associated with bats: Lagos, Duvenhage and Shimoni bat lyssaviruses. Little is known about the impact of these three diseases on humans, but we do know that Duvenhage’s lyssavirus is deadly: all three people known to have contracted this disease died (Van Thiel et al. 2009). With our ignorance of zoonoses in mind, Julie Shapiro (figure 9.10) decided to tackle the issue of bats and disease, specifically the link between land use, bats and the prevalence of bat-borne diseases. Shapiro completed her PhD in 2018 in Bob McCleery’s lab at the University of Florida. Since she was doing all her fieldwork in Eswatini, I was co-opted as a local adviser. In three gruelling field sessions, involving almost nightly excursions until 1:00 or 2:00 am, she 213

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Figure 9.10. Julie Shapiro conducting bat-related lab work on a field trip to north-eastern Eswatini. Photograph by Ara Monadjem.

captured hundreds of bats, which she gently bled, swabbed in and around the mouth, and then encouraged to provide faecal samples by placing them in cloth bags for an hour or two (figures 9.10–9.11). Once she had her samples, the bats were released, hopefully with nothing more than their dignity wounded. These samples were analysed, using the latest available technology, in the molecular lab of Anders Hansen (another of Shapiro’s advisers), a professor at the Natural History Museum, University of Copenhagen, Denmark. Shapiro recently discovered a number of new coronaviruses lurking in the bats that she sampled in Eswatini, and has established that the prevalence of various diseases in these 214

The Human Factor

Figure 9.11. Fezile Mtsetfwa (left) and Machawe (Maps) Maphalala entering data during a field trip at Mlawula Nature Reserve, Eswatini. Mtsetfwa was analysing calls of bats recorded by the same Anabat system that Julie Shapiro was using. Photograph by Ara Monadjem.

bats can be relatively high (Shapiro et al. 2021). This is, of course, of direct medical concern to humans, and may indirectly lead to the persecution of bats by local communities.15 It also complicates efforts to maximise the ecosystem benefits that these maligned creatures can offer. We thus have to find ways to balance the positives with the negatives. The complexity does not end here. Shapiro’s work linking land use and disease prevalence in bats is particularly interesting. Her preliminary analyses indicate that disease prevalence varies across land use. For comparison purposes, she categorised land use at her field sites as ‘protected’, ‘agricultural’, or ‘urban or peri-urban’. Bats from protected areas appeared to have the lowest prevalence of diseases, while those living in and around human habitation had the highest. If these results hold true then it could suggest that we (humans) are creating the conditions necessary for the flourishing of the very diseases that can harm us. Therefore, we can hardly lay the blame on the bats. They are merely responding 215

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to the changes that we have generated in our landscape. To persecute bats would be simply a ‘Band Aid’ solution, treating the symptoms but leaving the underlying causes untouched. A real and lasting solution will only come when we turn our attention to the causes themselves. *** In this chapter, I have offered a glimpse into the very complex world of human– wildlife interactions. Wild mammals have increasingly come into contact with humans as we have expanded our presence and influence ever more pervasively across the globe. Such has been our influence, in fact, that Earth has entered a new geological epoch, dubbed the Anthropocene, where our impacts will be visible to future civilisations in the geological record we leave behind. Human interactions with wild mammals are routinely viewed from the negative perspective of damage done to health, life or property. Mammals certainly are host to numerous deadly zoonoses that humans should be concerned about. However, as we continue to examine ecological processes more closely, we discover an ever-increasing diversity of ecosystem services provided by mammals that bring real, measurable benefits to humanity. Balancing these positive and negative benefits, and treating the roots of any problems rather than their symptoms, will be one of the great challenges of our generation of ecologists, agriculturalists and politicians.

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CHAPTER

10

The Sinking Ark?

T

his chapter was the most difficult for me to write, with many draft versions consigned to the trash before I finally settled on what you’re about to read. As you might imagine, the topic is a highly charged one for any lover of the natural world, let alone someone – like myself – who has dedicated much of their working life to protecting it. What’s more, in the process of writing it, I was obliged to confront many of the myths and misconceptions about conservation that I had once held, and had – mostly unwittingly – perpetuated. I will present these here on the assumption that many other conservationists face the same difficulties. I do not delve too deeply into the multifarious threats that biodiversity faces, however; these have been documented by many other authors and there would be little to gain from such an exercise, other than repeating what we all already know.

MYTHS AND MISCONCEPTIONS Ecologists are not conservationists The first myth I want to tackle is that ecologists are conservationists. In some ways, this is the core message of this chapter. Of course, some ecologists are conservationists, but the two are not necessarily the same – and most of the time they are definitely not the same. I was an undergraduate student at 217

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the  University of the Witwatersrand in Johannesburg (figure 10.1) at a time when the new subject of conservation biology had just reached critical mass and was quickly emerging from obscurity. Several new journals had been launched dealing exclusively with this theme, including two influential ones: Biological Conservation and Conservation Biology. If we were to leaf through an issue of either journal from the mid-1980s we would find articles with titles such as ‘Reproductive Biology of the Hawksbill (Eretmochelys imbricata) at Tortuguero, Costa Rica, with Notes on the Ecology of the Species in the Caribbean’ (Bjorndal et al. 1985); ‘The Distribution of Native and Introduced Landbirds on Silhouette Island, Seychelles, Indian Ocean’ (Greig-Smith 1986); and ‘Demographic Monitoring of Endemic Sand Dune Plants, Eureka Valley, California’ (Pavlik and Barbour 1988).1 These three titles clearly show what we thought conservation biology was about at that time. It was about studying the biology – typically including the spe­cies

Figure 10.1. The building that once housed the Department of Zoology at the ­University of the Witwatersrand, where I studied zoology in the late 1980s. This building now houses the School of Animal, Plant and Environmental Sciences (APES). Photograph by Chevonne Reynolds.

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population size, reproductive growth rate, diet and habitat requirements – of a species that was facing some sort of threat, and then making suggestions about how more habitat needed to be set aside or poaching pressure reduced to prevent it from going extinct. These suggestions were generally more hopeful than helpful because, in the real world, making such decisions involves dealing with people. Hence, conservation is primarily about how we deal with people, not how we deal with wildlife. The wildlife, let us remember, was doing just fine before we arrived on the scene. The upshot of this is that ecologists – who know how to track down and study even the most elusive of wild creatures – do not generally have the requisite skills to do meaningful conservation work. Yes, the information gathered by ecologists is absolutely vital for setting up effective conservation actions. But this information must be integrated into human social and cultural systems that ecologists typically have little understanding of – or interest in. Furthermore, conservation demands the requisite political skills to persuade governments and other local or international authorities to take appropriate actions. Equating conservation with ecology is thus not only incorrect but also harmful to the cause of preserving the planet’s future biodiversity. Understanding this simple truth involved a particularly difficult transition for me personally. Since my undergraduate days, I had identified myself as a conservationist. Letting go was not easy. However, this does not mean that ecologists, or other biologists, do not have a role to play in conservation. Quite the contrary. Real conservationists still need ecologists to ‘parameterise their models’, which in simple English translates to ‘provide valuable ecological input’. And some ecologists have made the transition to conservationists by acquiring skills in other areas, such as sociology, anthropology, law and resource economics. The important point for ecologists is that we need to grasp that ‘conservation is about people’ and adapt accordingly. Conservation is not the same as community development A second issue that I would like to confront is the role of the ‘local community’ in successful conservation. Everybody agrees that a protected area surrounded by an antagonistic community is going to have a harder time meeting its biodiversity conservation objectives than one that is on good terms with its neighbours. The goodwill of communities is important – but exactly how important? Should conservationists be expending time and energy in rural 219

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development projects, such as improved agricultural practices and healthcare? Communities surrounding African parks (as in figure 10.2) are often poor – in many cases, extremely poor. Average annual income in such communities may be a meaningless statistic, since ‘income’ may take completely non-monetary forms such as forest products that are used directly, or traded for other necessities. Few would disagree that people in such communities have lives that are drastically different from ours (that is, those of us who can afford to buy a copy of this book), with much tougher demands. These are people who may be without access to, say, running – let alone potable – water, modern medicine, or education for their children. Should we not care for them? Of course, we should. Decent humans should care about the plight of other humans, and where possible we should offer our assistance. But that is not the question I wish to ask. Rather, I am asking whether conservation funds (that is, those dedicated to ensuring the persistence of biodiversity) should be used to uplift

Figure 10.2. A rural community neighbouring the Gola National Park, Liberia. This would have been primary rainforest before it was clear-cut to make space for the houses and fields of this village. Photograph by Ara Monadjem.

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rural communities. Essentially, I am suggesting that we uncouple conservation issues from community development issues. Both are vital for the healthy future of humanity. And, in certain cases, dealing with one issue will automatically resolve the other. I am merely asking that we don’t assume a linkage from the start. Rather, let us examine each case independently. If community development is shown to be essential for effective conservation in an area, then by all means let us use conservation funds to assist the community. Conservation is not only about the management of protected areas The final issue that I want to raise is that conservation is not simply about the management of parks and nature reserves. These protected areas are nothing more than islands in a sea of humanity. Pick almost any park in Africa and it will have a burgeoning human population crowding its borders. Indeed, it may even have had communities within its borders who were uprooted after it was proclaimed, and moved to less productive land outside it. What’s more, many parks exhibit a distinct hard boundary. As an example, Bwindi Impenetrable National Park in Uganda protects beautiful montane and submontane forests, but on its eastern boundary neighbouring communities have cut every last forest tree right up to the park’s very edge, leaving a ‘barren’ agricultural landscape dotted with banana trees. By applying what we learned in chapter 4 about island fauna and the theory of island biogeography, we can see that these ‘islands’ – the protected area network of Africa – will not be capable of retaining their original biodiversity. Indeed, this decline was already predicted in the 1970s (Soulé et al. 1979). Predictions for the future of Africa’s large mammals are not encouraging. Table 10.1 shows the numbers of species that were present in east African protected areas in the 1970s alongside the number of species predicted to remain 50 years later (that is, in the 2020s). The figures are sobering. All the parks were predicted to lose at least one or two species over this relatively short time period, with the smaller ones – such as Marsabit and Nairobi national parks, both in Kenya – predicted to lose a greater proportion than the larger ones. Is there any evidence to bear out this predicted decline? To answer this question, we would need to know what species remain in each of these parks today – an exercise that, to the best of my knowledge, has not yet been conducted across the region. However, we do know that the populations of large mammals

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Table 10.1. Predicted declines of African large mammal species in east African parks, showing the extent of each protected area, the number of species that were known to occur in each of them in the 1970s, and the number of species predicted to remain in each area by Soulé and his colleagues (1979). The data are based on two of their models (model 2 and model 3), which have been shown to be the most accurate with respect to the situation in Tanzania (Newmark 1996).

Area (km2)

Number of species in the 1970s

Number of species predicted to survive to the 2020s (models 2 and 3)

Tsavo National Park (NP), Kenya

20 808

63

62, 60

Serengeti NP, Tanzania

14 504

70

69, 66

Ruaha NP, Tanzania

12 950

49

48, 47

Ngorongoro Conservation Area, Tanzania

6 475

40

40, 39

Murchison Falls NP, Uganda

4 040

42

41, 40

Amboseli Game Reserve (GR), Kenya

3 261

56

55, 51

Marsabit NP, Kenya

2 072

46

45, 43

Queen Elizabeth NP, Uganda

1 986

48

47, 44

Maasai Mara GR, Kenya

1 813

66

64, 57

Kidepo Valley NP, Uganda

1 259

44

43, 40

Mikumi NP, Tanzania

1 165

34

33, 32

Meru GR, Kenya

Park

222

1 021

58

56, 50

Aberdares NP, Kenya

590

43

42, 38

Mt Kenya NP, Kenya

588

31

30, 29

Lake Manyara NP, Tanzania

319

42

41, 36

Samburu GR, Kenya

298

56

54, 44

Nairobi NP, Kenya

114

56

53, 40

Ngurdoto Crater NP, Tanzania

54

38

36, 30

Olorgesailie NP, Kenya

0.2

11

10, 8

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in these parks have been declining rapidly (Craigie et al. 2010; Western et al. 2009). We also know that there have been large mammal extinctions in some of these parks. William Newmark, from the Natural History Museum of Utah in the USA, who is probably best known for his studies on the ecology of forest birds in the Eastern Arc Mountains of Tanzania, which he has been conducting for about three decades, has also published extensively on the ecology and conservation of the region’s mammals. In a landmark 1996 paper, he showed that large mammals had gone extinct in all six protected areas on which he could find information, with a proportionately larger decline in smaller protected areas (Newmark 1996). What’s more, these extinctions were in line with what had been predicted in the 1979 paper by Michael Soulé and his colleagues cited earlier. Sobering, indeed. However, accepting that parks are island havens for biodiversity does not quite go far enough. It misses the important point that the complex matrix of human landscapes surrounding these parks is itself suitable for many forms of life and ecological processes. We cannot afford to ignore this matrix. Fortunately, conservationists recognised this fact a couple of decades ago and embarked on what is known as transfrontier conservation. The rationale behind transfrontier conservation is quite simple: a larger, contiguous area under conservation is better suited to preserving biodiversity than a smaller or fragmented one. Conservationists poring over maps realised that many African conservation areas straddle national boundaries. Maasai Mara National Game Reserve in Kenya and the adjoining Serengeti National Park in Tanzania constitute one well-known example. So, why not manage such contiguous areas as one single transfrontier park? Unfortunately, the reality behind this apparently simple idea is more complicated than the theory. Although conservationists from different parks may be willing – indeed, eager – to help each other, there are numerous legal and management issues to be resolved when working not just with different park authorities but different national authorities! For example, what if one park allows hunting or participates in culling activities but the other park, by law, is opposed to this? If fences are dropped and animals move across the boundary, then authorities on one side may find themselves promoting objectives that they have long been fighting against. However, this is not the place to discuss transfrontier parks in detail. For now, I think we can agree that such cooperative activities are praiseworthy, and that in some quarters – for example, the Kgalagadi Transfrontier Park that spans 223

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the border between north-western South Africa and southern Botswana – they have already achieved great success. Instead, I would like to look at the next step that is already tentatively being taken: namely, implementing landscape-level conservation on a scale large enough for megafauna to provide meaningful ecological services. Linking protected areas on either side of national boundaries is all well and good, but it does not address the key issue of how to link unconnected protected areas – in other words, protected areas that are separated by modified habitats such as agricultural landscapes. Take the Kgalagadi Transfrontier Park, which consists of the former Kalahari Gemsbok National Park on the South African side together with the Gemsbok National Park on the Botswanan side. These two parks effectively merged in 2000 to become the transfrontier park that exists today (figure 10.3). This was a historically significant event that now allows 38 000 square kilometres of arid sandveld savanna to be managed as a single unit. However, this area was already protected, and merely creating the transfrontier area did not add to the protected area network of Africa.

Figure 10.3. The Kalahari is typically flat and open, with few trees to provide shade or shelter. Springbuck (Antidorcas marsupialis) are well adapted to surviving in this harsh landscape. Photograph by Mike Unwin.

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The question thus arises: how do we go about linking protected areas that are not contiguous and do not share common boundaries? Answering this question is, in my opinion, fundamental to addressing conservation issues in Africa. If we can figure out how to meet this challenge, we are on our way to success. If we fail, however, then the future of biodiversity conservation in Africa remains bleak.

THE KAZA CONCEPT A good starting point for responding to this challenge would be to find an example of an initiative that is already addressing this very question. But does such an initiative even exist? Is there a landscape that has multiple renowned, but non-contiguous protected areas scattered across it, with human settlement and agricultural lands filling in the matrix between them? In fact, there is such an example. It is called the Kavango-Zambezi Transfrontier Conservation Area or KAZA TFCA – or, more simply, KAZA. The KAZA TFCA, formally established in 2011, is an ambitious project that involves five participating countries – Botswana, Zimbabwe, Namibia, Angola and Zambia – and covers around 520 000 square kilometres, encompassing some 36 protected areas (Munthali et al. 2018) (figure 10.4). This is an enormous area, bigger than Zimbabwe and almost as large as Botswana, with an estimated human population of more than 2 million, which is larger than the population of Eswatini (1.2 million) and similar in size to that of Namibia (2.5 million). In other words, KAZA operates on the scale of an African country! The central tenet of KAZA is that African wildlife, especially the large mammals, is an important drawcard that attracts millions of tourists to Africa annually – at least it did so before the COVID-19 pandemic. The elephants and lions that tourists travel to see do not respect international borders and are therefore best managed based on ecological, rather than political, landscapes. Furthermore, allowing tourists easy access to the entire KAZA landscape will work to stimulate more tourists to visit other parks and game reserves in the region. To this end, Zimbabwe and Zambia have already established a UNIVISA that allows visitors to travel between these two countries on the same visa, and most international travellers do not need visas for Botswana or Namibia anyway. Hence, tourists can easily access and move between parks and reserves in four of the five participating countries. 225

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Zambia Angola

Zimbabwe Namibia

Botswana 0

100 200km

Figure 10.4. Map of the Kavango-Zambezi (KAZA) Transfrontier Conservation Area, showing the main protected areas included in KAZA (main map), and the central position of KAZA in southern Africa (inset map). All the transfrontier conservation areas in the region are shown in grey shading. Note that KAZA cuts across five southern African countries.

The mission of KAZA, as stated on their website, is ‘to establish a worldclass transfrontier conservation area and tourism destination in the Okavango and Zambezi River Basin regions of Angola, Botswana, Namibia, Zambia and Zimbabwe within the context of sustainable development’.2 KAZA is certainly well placed when it comes to promoting a world-class conservation area. Within its borders – especially in the Chobe-Hwange region of northern Botswana and western Zimbabwe – is the world’s largest population of African elephants (Loxodonta africana), some 200 000 strong. There are also vast herds of buffalo (Syncerus caffer) and zebra (Equus burchelli), and significant numbers of large predators, including lions (Panthera leo), leopards (Panthera pardus), cheetahs (Acinonyx jubatus), spotted hyenas (Crocuta crocuta) and African wild (or painted) dogs (Lycaon pictus). KAZA already includes a number of world-class wildlife destinations, including Chobe, Hwange and Kafue national parks, and 226

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the reserves and concessions of the Okavango Delta. With 36 protected areas, there is a large range of parks and reserves to choose from, providing diversity both for the plants and animals that inhabit them and the tourist who wishes to visit them. Wildlife dispersal corridors These 36 protected areas, however, are not contiguous. Most are separated by large tracts of communal land settled by small-scale subsistence farmers. Hence, one of the key first steps in the establishment of KAZA was to identify and create wildlife dispersal corridors. These corridors are vital if the ecological landscape of KAZA is to be maintained, and the extinction of wildlife within isolated parks averted. Here KAZA faces perhaps its biggest challenge: all these corridors pass through communal areas populated by poor, subsistence farmers who are struggling to eke out a living on agriculturally marginal lands. The last thing they need is roaming herds of elephants devastating their crops, or lions and other large predators mauling their livestock. But here also lies KAZA’s biggest opportunity: to truly empower and adequately remunerate conservation’s biggest potential ally – the communities that live around protected areas and bear the brunt of human-wildlife conflict (discussed in chapter 9). This isn’t going to be easy, especially since we are talking about five different countries, each with its own laws relating to land ownership and determining how local communities can benefit from the spoils of wildlife- and conservation-based tourism. At the very root, is the issue of rights over wildlife. Who can own – and therefore manage and hence benefit from – wildlife? How is this ‘ownership’ affected when wildlife crosses borders from one nation to another? And how are the profits from the sale of wildlife products, such as meat and trophies or ecotourism revenues, shared? Ecotourism and conservation Before I attempt to answer this question, I will briefly discuss the link between ecotourism and conservation.3 To some, the connection is self-evident and can be summed up as follows: the more tourists visit natural landscapes to observe indigenous wildlife in their natural habitats, the more money there will be available for conserving the very species and ecosystems that tourists have come to see – and the more money there will be for uplifting the local communities 227

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who would otherwise be disadvantaged by the loss to conservation of their potentially productive lands. This is all well and good in theory, but do we see it happening in reality? Are dollars spent on wildlife safaris, for example, being ploughed back into protecting native habitat from being transformed or degraded, and into the conservation of endangered species? Or is ecotourism simply a marketing ruse, perhaps akin to the ‘green’ branding of various consumer products, that serves to enrich the entrepreneurs involved in the business of selling safaris? In the words of Oliver Krüger, Professor of Animal Behaviour at Bielefeld University, Germany, is the role of ecotourism in conservation ‘panacea or Pandora’s box?’ (Krüger 2005). This debate may seem a rather tangential one for this book. I raise it here, however, because if ecotourism does not contribute to conservation, then we should not even be considering it as a means of conserving African mammals. Not surprisingly, there has been much debate in the scientific and lay literature on this issue, with polarised views. Part of the problem appears to be the lack of a clear, or at least universally accepted, definition of ecotourism.4 If you were to Google ‘definition of ecotourism’, as I did, you would probably encounter the following statement, or some derivative, on the first search page: ‘Ecotourism: travelling to relatively undisturbed or uncontaminated natural areas with the specific objective of studying, admiring, and enjoying the scenery and its wild plants and animals, as well as any existing cultural manifestations (both past and present) found in these areas’.5 However, you may also find any number of other definitions. One that I particularly like is as follows: ‘Low impact nature tourism which contributes to the maintenance of species and habitats either directly through a contribution to conservation and/or indirectly by providing revenue to the local community sufficient for local people to value, and therefore protect, their wildlife heritage area as a source of income’ (Goodwin 1996, 288). The reason that I like this definition is that it explicitly makes the link between tourism, conservation and local communities. Hence, if a tourism venture does not contribute to the conservation of biodiversity and benefit of local communities, then it is not, by definition, ecotourism. Returning to the question of whether ecotourism actually makes a positive contribution to conservation, the meta-analysis of Krüger (2005) showed that just 63 per cent of ecotourism ventures worldwide were ecologically sustainable, which was defined as not posing ‘a risk to the area or species in the foreseeable future’ (2005, 582).6 Even more worrying, just 18 per cent of the 228

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ecotourism ventures studied by Krüger were ecologically sustainable and made a positive contribution to conservation by, for example, stabilising or increasing the populations of an endangered species. However, despite these concerns, the Krüger study also observed that the proportion of ecologically sustainable ecotourism ventures was higher in Africa than in either South America or Asia, and that the presence of a flagship species, such as the African elephant, improved the odds further. From this, we can probably conclude that ecotourism is probably going to be good for conservation in a landscape such as KAZA. Rights to wildlife Countries that have granted local communities rights to wildlife are few. In contrast, title-deed or private landowners in many African countries already have well-entrenched rights over wildlife on their properties, which has fuelled the vibrant game-ranching industry present in countries such as South Africa. However, local communities on communal – non-title deed – lands typically are not legally permitted to benefit from extractive use of wildlife, such as trophy hunting or meat production, on their lands. An exception worth mentioning is Namibia, which in 1996 passed a law called the Nature Conservation Amendment Act (No. 5 of 1996) that granted wildlife and tourism rights to local communities, thus allowing them to benefit from the wildlife on their lands, particularly in partnership with the private sector (figures 10.5a–b). Such a partnership is of crucial importance where local communities do not have the capital needed to set up lodges and other expensive infrastructure required by ecotourism and hunting initiatives. Allowing local communities to participate equitably in wildlife-based ecotourism ventures has seen a complete change of heart among people living in such communities in Namibia. Whereas before, wildlife was seen, at best, as a nuisance and at worst a threat to their livelihoods, today these wild animals are viewed as an economic asset and one that is worth protecting. It is perhaps worth lingering a moment here to reflect on this. When we humans have ownership of something, we take care of it. When we don’t, we ignore it or abuse it. For decades, local communities have been viewed as threats to protected areas, with the lion’s share of conservation funding going to crime prevention schemes such as anti-poaching units. Of course, such units are an important part of any protected area and need to be supported and maintained. However, 229

(a)

(b) Figure 10.5. a–b. The Sorris Sorris Conservancy (top), a Namibian ecotourism venture, where visitors may see a variety of wildlife including plains zebra (bottom). Photographs by Seth Eiseb.

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most African parks have not been able to stem poaching, and wildlife continues to decline across the continent (Craigie et al. 2010). Most conservationists today will say that fundamental to wildlife conservation in Africa, and working handin-hand with anti-poaching initiatives, is giving local communities around protected areas equal access to the benefits, for example money raised from ecotourism ventures. Not only does this empower the communities by diversifying their economic activities away from doomed subsistence agriculture on marginal lands; it also means that each individual from the community has a stake in the wildlife on their lands. Many African countries, however, remain reluctant to hand local communities rights to wildlife. The reasons for this are diverse and beyond the scope of this book. Yet, unless we can turn this around, we are going to fail in our responsibility to conserve the planet’s biological diversity. Ironically, Africa probably is the world leader in community-based natural resource management; I say ‘ironically,’ because African countries, generally speaking, have been hesitant or even unenthusiastic to implement this home-grown and effective solution. Zimbabwe’s CAMPFIRE programme has come to define this approach. ‘CAMPFIRE’ stands for ‘Communal Areas Management Programme for Indigenous Resources,’ and the programme, which was initiated by the Zimbabwe government in 1989, is best known for the sustainable use of wildlife resources in buffer zones around Zimbabwe’s premier protected areas such as Hwange National Park (Child 1996; Taylor 2009). To be sure, CAMPFIRE has not been perfect and may even have failed in not significantly altering the livelihoods of subsistence farmers who make up the majority of the local communities participating in the programme (Mutandwa and Gadzirayi 2007). However, I get the feeling that the problems here are not because of how CAMPFIRE was originally conceived but rather with how it has been implemented, with insufficient involvement of local communities at some key stages, meaning that the benefits did not reach all community members effectively. I have not personally been involved in KAZA (or the CAMPFIRE programme, for that matter) and only know some of the key players by their reputations. However, I must confess that I am taken by the concept. All political borders are artificial, but those in Africa are extremely so, given the way in which the continent was carved up by European colonial powers during the ‘Scramble for Africa’ (1881–1914). Thus any initiative that seeks to foster cross-border collaboration and ease the considerable pain of travelling across borders in Africa is appealing to me. And managing whole ecosystems and landscapes, rather than 231

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isolated pockets of natural habitat surrounded by inhospitable spaces, is also appealing. Finally, involving local communities in a meaningful and equitable fashion, and seriously addressing the issue of poverty alleviation, is the cherry on the top. I sincerely hope that KAZA succeeds and that this becomes a model for the conservation of wildlife in other African landscapes. To date, the project has yet to demonstrate its success, particularly in relation to cross-border management and empowering or involving local communities. In the interim, I will be watching and supporting from the sidelines. Assuming that KAZA succeeds – and I predict that it will – what does this mean for conservation initiatives elsewhere in Africa? Are there any take-home lessons that could be applied to conservation in, for instance, my home country of Eswatini? After all, KAZA is unique in two very important respects. First, it has an abundance of flagship species – ‘the Big Five’ and many more – that can easily be seen in most of the region’s parks. Second, although a large number of people reside within the borders of the KAZA TFCA, the human density is on the low side in most of the region, with approximately 72 per cent of the land being under conservation. The presence of flagship species and good neighbourly relations are vital conditions for ecotourism to contribute to biodiversity conservation (Krüger 2005). What can be done when either flagship species are not present (or not easily observed), or bordering local communities are unfriendly and/or so populous that benefits derived from conservation initiatives will not meaningfully improve their livelihoods? I would suggest that this is the norm in African countries, and that KAZA is an exceptional case. In such situations, is there anything else we can do to ensure the continued existence of Africa’s iconic mammals and its other biodiversity?

CONSERVATION IN ESWATINI I come from the little country of Eswatini that is perhaps as far removed as possible from the KAZA concept. Indeed, it is more typical of the situation across much of Africa, where large tracts of wilderness no longer grace the landscape. Can we still conserve biodiversity in such landscapes devoid of ‘the Big Five’ and other charismatic mammal and bird species? I will try to answer this question using Eswatini as an example, but the principles are applicable to other such regions of the African continent. 232

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Eswatini is a tiny country wedged between South Africa to the north, west and south, and Mozambique to the east (figure 10.6). Indeed, with an area of just 17 364 square kilometres, it is smaller than many protected areas in southern Africa, including the Kruger, Kafue and Namib-Naukluft national parks. Yet, more than 3 400 species of plant and 850 species of vertebrate animal have been recorded within its borders (Braun et al. 2004; Monadjem et al. 2003). This diversity arises from the wealth of habitats created by the steep elevational – and hence climatic – ­gradient from the mountainous west to the low-lying east of the country. Although the total human population (1.2 million people) may sound rather small for a country, its density, at approximately 70 persons per square kilometre, is high. This creates high pressure on the remaining natural lands, nearly all of which are either in protected areas or on privately owned (title-deed) ranches. Almost all the remaining large

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Figure 10.6. Map of Eswatini showing the proclaimed protected areas in the country (dark grey shading): 1) Malolotja Nature Reserve; 2) Hlane Royal National Park; 3) Mlawula Nature Reserve; 4) Mkhaya Game Reserve; 5) Mlilwane Wildlife Sanctuary; and 6) Mantenga Nature Reserve. Also shown (pale grey shading) are other areas of conservation importance but that have not been proclaimed.

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mammals in Eswatini occur on these protected or privately owned lands. That is not to say that there is nothing left to conserve outside protected areas; far from it. There are still beautiful river gorges with natural forests supporting a rich plant and bird diversity to be found on community land, also called Eswatini Nation Land (ENL), which covers roughly 60 per cent of the country. However, biodiversity has not been managed well on ENL; in fact, mostly it hasn’t been managed at all, but has simply been exploited and overused, with no checks and balances in place to ensure continuity into the future. Since large mammals are mostly gone from ENL, biodiversity resource use revolves around plants and smaller animals. Plants are generally used for medicinal purposes and for timber, while small and medium-sized mammals and certain birds – such as vultures – have been used for supplementary protein and for preparing potions for dubious traditional uses, such as predicting the future. Perhaps the biggest threat to the remaining native forested habitats is the cultivation of dagga (marijuana), which is illegal and hence carried out in hidden locations.7 From the outside these forests may appear pristine; only upon entry is it apparent just how degraded they have become as a result of being cleared for dagga cultivation. What is the future of mammal conservation in such an environment? Are large mammals doomed to surviving only in heavily managed and isolated protected areas, perhaps with regular reintroductions to fight off in-breeding depression? Or could we apply lessons learnt from KAZA and CAMPFIRE to Eswatini? At this point, we enter uncharted waters. Thus anything I write about this issue is untested and based purely on my personal opinion. In some respects, Eswatini is not entirely comparable to other African countries because the protected areas are relatively well managed. This is particularly so on the properties run by Big Game Parks, which manages Mlilwane Wildlife Sanctuary, Hlane Royal National Park, Mkhaya Game Reserve and KaMsholo Bushveld Safaris. Wildlife is prolific in these parks and elephant and rhino poaching is basically absent, which is something of an anomaly on the continent. This is certainly a tribute to the work of Ted Reilly (figure 10.7) and Liz Reilly, who pioneered wildlife conservation in Eswatini, with strong support from the monarchy. The remaining government-run parks in the country fall under the Eswatini National Trust Commission, which has worked hard to stem the tide of poaching on its properties; these include Malolotja, Mlawula and Mantenga nature reserves. 234

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Figure 10.7. Ted Reilly, doyen of conservation in Eswatini. Photograph by Danny Steyn.

Can community-based conservation thrive in Eswatini? The basic question Eswatini faces is whether community-based conservation can thrive under the pressures to which community land is subject. None of the parks I have mentioned above are large, the largest being around 170 square kilometres. But all these parks have a burgeoning human population surrounding them. How can such small parks produce sufficient revenue to allow them to effectively manage themselves, while also contributing to the welfare of neighbouring communities? In my opinion, we are asking too much of these parks, most of which cannot – or have not been able to – cover their 235

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own basic operational costs, let alone turn a profit to be shared with the communities that surround them. Perhaps we are looking at this from the wrong angle. We are looking at how established protected areas could use the profits they generate within their borders to benefit surrounding communities. Maybe we should be looking at how these protected areas might assist local communities to conserve wildlife and biodiversity outside the areas of protection. In all honesty, there are currently no examples of working community-based conservation initiatives in Eswatini. Yes, there is the Shewula Nature Reserve, which shares its southern border, across the Mbuluzi River, with Mlawula Nature Reserve and Mbuluzi Game Reserve, and is owned and – to a limited extent – managed by the Shewula community. It runs a lovely little camp called the Shewula Mountain Camp, with sweeping views of the lowveld of Eswatini. Before COVID-19, this camp was a popular destination for tourists. But Shewula cannot by any stretch of the imagination be said to actively manage its wildlife. Indeed, wildlife is negligible on the Shewula side of the Mbuluzi River, yet it abounds in the Mbuluzi Nature Reserve on the other side of the river. What is more, Mbuluzi Nature Reserve is plagued by almost nightly intrusions of poachers, most of whom come from the Shewula community. What can be done to turn the community around and bring them into the fold of conservation? Again, I have no answers to offer. However, I would like to draw attention to something that often does not receive the consideration that it deserves in conservation circles, and that is the role of culture in promoting biodiversity conservation. Earlier in this chapter, I highlighted the direct link between humans and conservation action, and stated that most endangered species of plant and animal are endangered because of humans. The corollary of this is that humanity is the biggest threat to biodiversity on this planet. Many human societies around the world today survive and even thrive in an apparent disconnect with the ‘natural’ world. We buy our food in supermarkets, unaware of its origin in distant farmlands. We visit zoos and safari parks but would not be able to survive two days in the ‘wild’ without our first-world camping gear and food supplies. This disconnect tends to be greater in urban and advanced agricultural societies, however, and there are still many African communities that buck the trend. I have had the privilege of spending time across Africa with some amazing African guides who have led me through forests and savannas, and taught me loads of things about these ecosystems. I have learnt as much about 236

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plants and animals in such field classrooms as I have in any conventional classroom. Many of the people who were my field teachers would today be labelled as ‘poachers’ – indeed, many of them had been poachers – but that does not diminish their wealth of knowledge. Why are we failing to harness the expertise and experience of such people to work with us in conserving the continent’s mammals? Swati society, like much of the world, comprises a pleasant mix of urban, semi-urban and rural folks. Many of those raised in rural homes have a good working knowledge of biodiversity in their areas, including edible wild fruits and plants of medicinal importance. This knowledge has slowly diminished in recent decades as rural populations have increasingly found work in the urban centres of Mbabane and Manzini. However, regardless of whether a Liswati has had a rural or urban upbringing, culture is highly valued, respected and adhered to.8 And anyone who has spent even a short time in Eswatini will know that this culture is deeply rooted in the nation’s biodiversity. From the leopard skins and ligwalagwala feathers that appear in the regalia of royalty, to loin skins called emajobo worn by men, and the collection of reeds or sicklebush by girls or boys in annual ceremonies, nearly every cultural event involves the use of some indigenous plant or animal (figure 10.8).9 Furthermore, Emaswati do not follow culture as a superficial, ‘once-in-a-while’ nostalgic trip to the past. Culture permeates Swati society, and you will regularly hear Emaswati proudly proclaiming that ‘we have kept our culture’. This rich cultural heritage would fade quickly and vanish altogether if the plants and animals on which it is based were to disappear. Perhaps this is the key to conserving biodiversity in Eswatini? Perhaps Emaswati are not aware of the threats to their biodiversity, and do not realise that much of it has already disappeared from the country. Maybe conservation initiatives need to recognise this visceral grassroots bond between Emaswati and biodiversity, and build on this. *** One thing that I have learnt in my almost 30 years of teaching is that wellformulated and logical arguments are all well and good, but you cannot rely upon them to sway people’s hearts. We humans are more instinctively receptive to arguments based on emotion than those based on cold logic. Africa certainly has its share of conservation problems, but for too long we have tried to address these using actions and ideas derived from other parts of the world. 237

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Figure 10.8. Themb’a Mahlaba in traditional attire. Photograph courtesy of Themb’alilahlwa A.M. Mahlaba.

Perhaps Africa needs its own home-grown conservation model that builds on the links and connections already present between African societies and the environments in which they have evolved. I believe that this will ultimately be the way to turn the conservation failures across the continent into successes. I do not know exactly how this will come about. No doubt the road will be a bumpy one, with setbacks along the way, and we may have to accept that further losses to biodiversity are inevitable before the decline is arrested. But I do think that for most of Africa, addressing the role of local communities is the single most fundamental step that needs to be taken. Once these communities are genuinely and directly involved in conservation, in a way that offers both ownership and benefits, addressing all other challenges will, I believe, become possible. Providing rights to utilise wildlife resources for these communities 238

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is a necessary precondition, but it is not enough in itself. Meanwhile, as we wait for conservationists to find an answer, we ecologists can continue to amass the data and conduct the studies that help us understand this richly diverse continent, while all of us continue to marvel at the beautiful array of mammals that it holds.

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GLOSSARY

Abiotic Refers to the physical, as opposed to biological, conditions in which animals and plants have to live out their lives. Accession number In taxonomy, a unique number assigned as an additional means of locating and identifying a specific item deposited in a museum. Adaptive radiation In evolutionary biology, a process by which organisms diversify from one ancestral species into multiple new forms, specifically when an environmental change makes new resources or niches available. Allele Any of two or more alternative forms of a gene that arise by mutation and occur at the same place on a chromosome. Allopatric Of related species or populations of animals or plants, occurring in separate non-overlapping geographical areas. Animalivorous Feeding and subsisting entirely upon animals (including invertebrates and vertebrates). Compare with carnivorous, which specifically refers to those species that feed on vertebrates. Basal In systematics, taxa associated with the base of a phylogenetic tree (and hence more ‘primitive’). Basal metabolic rate The amount of energy expended (number of calories burned) by an endothermic animal when at rest. Base pair A fundamental unit of double-stranded nucleic acids, comprising two nucleobases bound together by hydrogen bonds. Base pairs form the building blocks of the DNA double helix. Biome A large area characterised by its vegetation, soil, climate and wildlife. There are five major types: aquatic, grassland, forest, desert and tundra; each can be further divided into more specific categories.

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Biotic In an ecosystem, describes living or once-living components, such as animals and plants. Circadian Of a natural or metabolic process: following a 24-hour (daily) cycle. Clade A group of different organisms all descended from a common ancestor, including the ancestor itself. Coevolution The process of reciprocal evolutionary change, whereby two or more species influence each other’s evolution through natural selection. Convergent evolution A process whereby unrelated organisms independently evolve similar traits through adaptation to similar environments or ecological niches. Cryptic species Two or more species that have been (mistakenly) classified as a single nominal species due to their close morphological similarities. Cursorial Of an animal that is adapted for running. Depauperate Of a fauna, flora or ecosystem, lacking in number and/or variety of species. Detritivore An animal that feeds on dead organic material, especially plant detritus. Diastema: A gap or space between the incisors and cheek teeth. Diploid Refers to animals (or plants) with chromosomes arranged in pairs. Compare with haploid, which refers to animals with single chromosomes. Divaricate Of plant morphology, diverging from the stem at a wide angle; divaricating growth patterns are typically zigzag in appearance and thus produce tightly interlaced shrubs or trees. Ecosystem services Benefits to humans, such as plant pollination or medicinal resources, produced by the natural environment and the organisms that inhabit it. Ectothermy Animals’ capacity to control their body temperature through external environmental factors. Compare with ‘Endothermy’. Emergent property Exhibited by a complex system, such as a collection of organisms living together, but cannot be recreated by the summing of the individual components. Endemism Of a species, native to a single defined geographical region.

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Glossary

Endothermy Capacity to maintain a favourable body temperature largely through internal bodily processes; endotherms are often (misleadingly) described as ‘warm-blooded’. Compare with ectotherms that control body temperature through external environmental factors. Environmental gradient A gradual change in an environment over space and/ or time through changes in abiotic factors, such as altitude and temperature. Changes in an environment’s biotic components, such as its plant communities and animal populations, are related to these gradients. Ethnobotany The study of the historical and cultural relationship between humans and plants. Functional group See ‘Guild’. Guild In ecology: a collection of species that exploit the same environmental resources (such as food and shelter), or different environmental resources in a similar way; members of an ecological guild need not be taxonomically related or occupy the same ecological niche. Mammalian examples of guilds include ‘fruit-eating bats’ (which are taxonomically related) and arboreal frugivores (which consist of taxonomically unrelated squirrels and primates). Haploid Refers to animals (or plants) with single chromosomes. Compare with ‘Diploid’. Herbivory The consumption of plant material by animals; herbivores are animals adapted to eating plants. Heterothermy Refers to animals that do not maintain a constant body temperature. Compare with ‘Homeothermy’, which refers to animals that maintain constant body temperatures. Homeothermy Refers to animals that maintain a constant body temperature. Compare with ‘Heterothermy’. Hypervolume A region of space defined by more than three dimensions. Although we cannot represent hypervolumes in three-dimensional space, and therefore they are difficult for us to visualise or imagine, they are useful mathematical tools used extensively in ecological research. Ichthyology A branch of zoology concerned with the study of fishes. Immature An individual of any animal species that has not yet reached breeding maturity.

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Inbreeding depression Reduced biological fitness – and therefore reproductive success – in a given population of animals as a result of inbreeding (the breeding of related individuals). Irruption An abrupt increase (and sometimes consequent movement) of an animal population. Also referred to as an outbreak. Loreal scale A scale on the head of a reptile that lies between its eye and nostril, and is absent in snakes in the family Elapidae that includes cobras and mambas. Mesic Of an environment or habitat having a high supply of moisture. Mesocarnivore A medium-sized carnivore, such as jackals, servals, genets and civets. Mitochondria Organelles, which are specialised structures within a living cell, found in large numbers inside the cells of most living organisms that produce energy for the cell. Monophyletic A group of organisms descended from a common evolutionary ancestor or ancestral group, especially one not shared with any other group. Monotypic Having only one type or representative. For example, a monotypic genus contains just one species. Morphology: The physical form and structure of an organism; the branch of biology that deals with form and structure. Morphotype Any of several morphologically different types of individuals within one population of the same species. Obligate scavenger An animal that relies for its food entirely or almost entirely on carrion. Pelage The coat (fur, hair, or wool) of any mammal. Pelagic Relating to any organism living primarily in the open ocean, away from coastal and terrestrial habitats. Phylogeny In systematics, the relatedness of taxa, typically presented as a branching tree, with more closely related taxa positioned closer together on the terminal tips of the tree. Preorbital scale The scale immediately in front of the eye of a reptile or fish. Range state Any nation that forms part of an organism’s natural geographical range.

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Ratite Any of a group of large, flightless birds that lack a keeled breastbone. Today’s ratites comprise ostriches, rheas, emu, cassowaries and kiwis. Recruitment In population dynamics, the process through which new individuals are added to a population, whether by birth and maturation or by immigration. Sister species Closest related species of a given organism in an evolutional tree. Species pump A large-scale environmental event, such as the formation of a mountain range or an island, that drives the process of speciation and results in an increased rate of species production. Stem group A grouping of organisms comprising an ancestor and all its descendants, excluding living representatives of that group. Subspecies A taxonomic category that ranks below a species, and normally refers to a geographically isolated population that is distinct in some relatively minor way, but not sufficiently distinct to be called a species. Systematics The study of relationships among different groups of organisms and their evolutionary development. This includes classification systems and nomenclature of organisms. It studies the distinctive characteristics of species and how they are related to other species through time. Taxon A taxonomic group of any rank, such as a species, family or class. Plural: taxa. Taxonomy The branch of biology that deals with the classification and naming of organisms. Trophic level A particular position in the food chain. If we follow the flow of energy through a simplified food chain, we see that it begins with plants that synthesise their food from the sun, then moves to herbivores that feed on plants and finally reaches carnivores that eat the herbivores. In such a system, plants would constitute one trophic level (producers), herbivores another level (primary consumers) and carnivores yet another level (­ secondary consumers). Tympanum An eardrum (tympanic membrane). Ultrasound Sound waves at frequencies greater than the upper limit of the audible range for humans (approx. 18 kHz). Many animals can produce and hear sounds in the ultrasonic frequency range.

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Ungulate Any of a group of medium-sized to large mammals, most of which are herbivorous and have hooves. Typical herbivores include cattle, deer, sheep, pigs, antelope, camels, rhinoceroses and horses. Vomeronasal organ An organ of chemoreception, located in the main nasal chamber, that works by detecting moisture-borne odour particles and is part of the olfactory system of reptiles.

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CHAPTER 1: A CONTINENT OF PLENTY

1 2

3 4

5 6 7

A taxon is any unit (for example, a species, family or class) used in the science of biological classification or taxonomy; plural = taxa. The total number of bat species from Madagascar has been put at as many as 47 species, but the ‘endemic’ Nycteris madagascariensis (Malagasy slit-faced bat) has since been removed from the list (Demos et al. 2021). The IUCN Red List website is a very useful electronic tool for mammologists and conservationists in general (IUCN 2019). Examples of families might be Canidae (dogs and their relatives) and Felidae (cats and their relatives), while examples of orders might be Carnivora (carnivores including Canidae and Felidae) and Rodentia (rodents that include squirrels, mice and rats, porcupines, and so on). There are 11 species of African vulture, if the cinereous vulture (Aegypius monachus), which is now thought extinct on the continent, is included. This number increases to 50 species of bat if we include the landscapes around Gorongosa National Park, but this far more extensive area would not be comparable with Mount Nimba. Some claims suggest that up to 2 900 people are killed annually by hippopotamuses. This is 2 900 too many, of course, but it is as nothing compared to the 650 000 people who die annually in Africa from malaria, carried by mosquitoes, and considerably less than the approximately 14 000 people killed annually on the roads of South Africa, alone. (See https://www.dsclaw.co.za/articles/time-to-sit-up-14000-south-africans-­dieon-our-roads-every-year/.) Hippopotamuses can be dangerous, but motor vehicles are much more so.

CHAPTER 2: THE SPECIES CONUNDRUM

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An allele is ‘one of two or more alternative forms of a gene that arise by mutation and is found at the same place on a chromosome’ (Hobson 2004). A subspecies is a taxonomic category that ranks below a species, and normally refers to a geographically isolated population that is distinct in some relatively minor way,

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but not sufficiently distinct to be called a species. When zoologists use the Latin trinomial (three-part name), as in the case of Naja nigricincta woodi, they are referring to a subspecies. Sequencing is the act of reading the script of the DNA molecule, which consists of millions of A, T, G and C (adenine, thymine, guanine and cytosine) base pairs. DNA is a double helix, with one strand the exact mirror image of the other strand, brought about by the fact that A only bonds with T, and G only with C. Hence, a sequence of DNA reads as a series of As, Ts, Gs and Cs strung out in a long sentence such as ‘AATGCCGCTCAA’. This division of sex cells is called meiosis in this case; it is called mitosis when the DNA is being copied to produce non-sex cells. Nuclear genes are situated in chromosomes in the nucleus of each cell, whereas mitochondrial genes are situated in a single circular chromosome in each mitochondrion. The order Squamata was traditionally divided into Serpentes (snakes) and Lacertilia (lizards). This organisation of the Squamata is no longer correct and snakes are now recognised as being specialised lizards. Although the names ‘Serpentes’ and ‘Lacertilia’ are no longer valid, the logic of this argument is not affected. This semi-aquatic rodent forages in small forest streams across tropical Africa (Giarla et al. 2021). Vahatra is dedicated to the study and conservation of Madagascar’s biodiversity. See http://www.vahatra.mg (accessed 14 July 2022).

CHAPTER 3: THE HISTORY OF AFRICA’S MAMMALS

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The sequence of the periods relevant to mammals between the two mass extinctions is as follows: Permian, Triassic, Jurassic and Cretaceous. These geological epochs are discussed in more detail in chapter 9. This planet has always belonged to very small creatures, particularly bacteria, which continue to rule it today. Bacteria can survive without plants or multicellular animals (or even unicellular animals such amoebas), but none of these ‘advanced’ creatures could survive without bacteria. In fact, the ‘eukaryotes’ (which include all life forms other than bacteria and are distinguished by nucleated cells) evolved by a symbiotic association between two bacterial cells, resulting in the development of mitochondria and chloroplasts – essential structures for the functioning of cells. If we removed mitochondria and chloroplasts from eukaryotic cells, then the survival of advanced organisms would be reduced from days to seconds. We need to stop kidding ourselves about our ‘dominance’ over nature. The term ‘group’ refers to a geological stratum or layer of rock, and ‘supergroup’ simply means an aggregation of related layers that were deposited at different stages of geological history. Hence the Beaufort Group, together with the Dwyka Group, Ecca Group, Stormberg Group (better known by its subdivisions as the Molteno, Elliot and Clarens formations), and Drakensberg (and Lebombo) Group collectively make up the Karoo Supergroup, with the Dwyka Group deposited first and the Drakensberg Group last. Animals that maintain their core body temperature are referred to as homeothermic, whereas those that allow their core temperature to fluctuate are heterothermic. The order Squamata includes lizards and snakes, and is by far the largest group of extant (that is, currently living) reptiles.

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Remember that life first evolved in an aquatic (and almost certainly marine) environment, and that until the Cretaceous Terrestrial Revolution, diversity of life had always been higher in the oceans than on land. A clade refers to the fact that all its descendants share a common, recent ancestor – ‘recent’ at least in relation to other clades (that is, they are monophyletic). The Tethys refers to the sea that formed between Laurasia and Gondwana, but it has been squeezed shut by the northward movement of Africa towards Eurasia. For much of the past 90 million years, Africa has been completely surrounded by water, this isolation having been broken only on a small number of occasions that allowed fleeting contact between Africa and Eurasia. All that remains of this once vast ocean is the Mediterranean Sea. Caviomorphs are a clade of hystricognath (that is, porcupines, guinea pigs and their relatives) rodents restricted to the New World. Platyrrhines are New World monkeys; catarrhines are monkeys restricted to the Old World.

CHAPTER 4: ISLANDS AS SPECIES FACTORIES

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Oceanic islands (for example Mauritius), as opposed to continental islands (such as Borneo or Sumatra), have never been connected to the mainland; they have developed in situ (that is, in their original places), usually as a result of volcanic action. 2 Mayotte is an overseas department of France; the remaining three islands form a single nation, the Union of the Comoros. 3 All three of these islands are part of the United Republic of Tanzania; the first two make up the archipelago known as Zanzibar. 4 São Tomé and Principe form an independent country, whereas the other two islands belong to Equatorial Guinea. 5 I am excluding cetaceans (whales and dolphins) and pinnipeds (seals) which, by their marine nature, do not view these islands as remote or inhospitable, and the introduced house mouse Mus musculus and domestic cat Felis silvestris catus, which reached these islands by human agency. The domestic cat was eradicated from Marion Island (part of the Prince Edward group), and there are plans afoot to eradicate house mice from Gough Island (part of the Tristan da Cunha group). Whether mice can also be eradicated from Marion Island using current methods is not yet clear. 6 Many other mammals have been introduced to the Canary Islands, including rodents, rabbits, hedgehogs and shrews. 7 With the exception of one species Miniopterus griveaudi (Goodman et al. 2010). 8 The LGM refers to the peak of the most recent ice age, dated around 20 000 years ago. 9 Some say that the lesser Mascarene flying fox roosted in hollow trees and that deforestation caused its extinction (IUCN 2019). In either case, the principal agent of its extinction was Homo sapiens. 10 At present, the Mozambique current, which is configured north to south, is such that it would be practically impossible to complete the journey across the Mozambique Channel from mainland Africa to Madagascar. However, ocean currents were different in the past due to the different positioning of continents. Using simulation models, it has been suggested that from the Eocene to the Miocene (when all terrestrial mammals colonised the island) this current ran from north-west to south-east, that is, from the east African coastline to Madagascar, facilitating colonisation. The modern

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configuration of the current began around 15 million years ago and may explain why no further colonisation events have taken place more recently (Ali and Huber 2010; Krause 2010). CHAPTER 5: EVOLUTION ON THE AFRICAN MAINLAND

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We will return to the subject of the blue antelope in chapter 10. In fact, the Afar region extends across three countries: Ethiopia, Eritrea and Djibouti. Technically, the Gregory Rift includes the sections from Ethiopia, through Kenya to northern Tanzania. A separate population occurs in the miombo woodlands of south-central Africa. Hylomyscus kerbispeterhansi was named in honour of Julian Kerbis Peterhans, a leading expert on the Albertine Rift who has described many new species of small mammal from across Africa. Species groups do not describe a taxonomic level such as genus, subgenus and so on. Instead, taxonomists use species groups to categorise closely related species within a genus. This is especially useful in making sense of taxonomic relationships in large genera such as Hylomyscus (with 18 species currently recognised). In our example here, H. denniae is in the denniae group while H. kerbispeterhansi is in the anselli group. In ecology, species richness is defined as the number of species (and is usually used with a particular site or region in mind). In this sense, richness is a simple count of the species present. It is important to note that to ecologists, species richness and species diversity are not interchangeable terms; the latter refers to differing proportions of co-occurring species within a community (that is, population sizes of the different species need to be taken into account). A diverse community has a relatively large number of species that occur at similar densities, whereas a community numerically dominated by one or two species has lower diversity. The Dahomey Gap has come about by natural processes, predominantly the particularity of the regional climate, which has resulted in local aridity and hence savanna (as opposed to forest) vegetation. These four species are, in the order that they were described: Pseudoromicia roseveari (Monadjem et al. 2013); Pseudoromicia isabella (Decher et al. 2015); Nycticeinops happoldorum (Hutterer et al. 2019); Pipistrellus simandouensis (Monadjem, Richards et  al. 2021). Note that three have different genera from those they were originally described in. This is reviewed in Monadjem, Demos et al. (2021) and will not be elaborated here. A fifth new species, Miniopterus nimbae, is a split of an existing species (M. inflatus) that was previously known from Mount Nimba (Monadjem et al. 2019). An isolated population of western gorillas, known as the Cross River gorillas, also occurs in the border region between Cameroon and Nigeria and is recognised as a separate subspecies (Gorilla gorilla diehli). A second genus of jerboa (Allactaga) occurs in Libya and Egypt. Chromosomal analysis requires counting the numbers of chromosomes, or examining their physical structure, whereas molecular analysis refers to sequencing the order of the four base pairs in genes (as discussed in chapter 2). A palaeo-lake is an ancient lake that no longer exists. The remnants of this lake can be seen in Botswana’s Makgadikgadi Pans (Sua, Nxai and Ntwetwe).

Notes

14 Banks of rivers are designated as left or right in relation to the direction of flow, that is, the right bank is on your right only if you are facing downstream! 15 Over evolutionary time and assuming no mixing with other populations, we would expect the chimpanzees in the Upper Guinea rainforests to diverge sufficiently to become a separate species. But the difference is too slight to designate species-level distinction today, although at least one study (Morin et al. 1994) disagrees and argues for specific recognition for the western chimpanzee as Pan verus. 16 We will hear more about Herwig Leirs in chapter 9. 17 By comparison, just 15 species were recognised in Mammals of Africa, published two years earlier by Jonathan Kingdon and his colleagues (Kingdon et al. 2013). Since the publication of our book in 2015, Taylor has described another new species, Otomys willani (Taylor et al. 2019), bringing the total to 32 species in the genus.

CHAPTER 6: GIANT MAMMALS SHAPING THE LANDSCAPE

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The savanna elephant of Africa is the largest of the megafauna alive today, with the heaviest individual on record weighing 6.5 tons, but more typically 5 tons for a large male and 3 tons for a large female. The Pleistocene epoch stretches from about 2.5 million to 12 000 years ago and covers all 17 recent ice ages, up until the beginning of the latest interglacial, when agriculture was first adopted by humans. Note that the order Cetartiodactyla includes the marine whales and dolphins. These were previously placed in the order Cetacea. However, molecular studies clearly show that they are nested within the even-toed antelopes group, previously in the order Artiodactyla, with hippopotamuses being more closely related to whales than to other antelopes. This necessitated the combining of these two groups into the new order Cetartiodactyla. Perhaps even more surprisingly, there were even a few enormous rodents at this time, the largest being the recently discovered Josephoartigasia monesi that probably weighed just under a ton (Rinderknecht and Blanco 2008). Homo sapiens literary translates as ‘thoughtful man’. This is a rather unfortunate moniker in my opinion, considering how little true thought we display as a species – as opposed to memorising and blindly adopting the ceremonial and cultural practices, norms and standards of our ancestors. Homo erectus appeared about 2 million years ago and survived until around 200 000 years ago, although some claim that the ‘pygmy’ humans that died out on Flores, Indonesia, as recently as 30 000 years ago might have represented the last lineage of this once widespread species (Brown et al. 2004). Five species in the genus Cylindraspis occurred on the three Mascarene Islands, and all five are extinct. The exact date of human arrival on Madagascar is not known, although there is clear evidence of human presence at least 2 000 years ago (Douglass et al. 2019). A trophic level is a particular position in the food chain. If we follow the flow of energy through a simplified food chain, we see that it begins with plants that synthesise their food from the sun, then moves to herbivores that feed on plants and finally reaches carnivores that eat the herbivores. In such a system, plants would constitute one trophic level (producers), herbivores another level (primary consumers) and

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carnivores yet another level (secondary consumers). Under closer analysis, the situation is far more complicated and involves many additional levels, including multiple carnivores as well as detritivores and others. 10 Body size also influences this relationship, by enforcing a higher metabolic rate per unit of mass on smaller species. This is discussed more fully in chapter 7. 11 A camera trap is simply a camera fitted with a motion sensor. When an animal moves past the lens it ‘trips’ the shutter and a photograph is taken. This is an effective method for assessing the presence of secretive and nocturnal species such as leopards. Bat detectors can record the ultrasonic calls of bats. Since the calls of many bats are identifiable to genus or species level, it is possible to work out which species are present in an area by simply setting up a bat detector to record through the night. CHAPTER 7: A PLACE FOR EVERY SPECIES

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An emergent property is one that is exhibited by a complex system such as a collection of organisms living together, but that cannot be recreated by the summing of the individual components. 2 A hypervolume is a region of space defined by more than three dimensions. Although we cannot represent hypervolumes in three-dimensional space, and therefore they are difficult for us to visualise or imagine, they are useful mathematical tools used extensively in ecological research. 3 Although the competitive exclusion principle is given this grand title, it is difficult to find good examples of it operating in the natural world on an evolutionary scale. 4 There are two measures that zoologists use to describe the relative shape of the wing: wing loading and aspect ratio. The former is calculated by taking the mass of the bat and dividing this by its wing area; the latter is calculated by taking the square of the wingspan and dividing it by the wing area. Fast-flying bats typically have high wing loading and high aspect ratio, whereas bats that rely on manoeuvrability typically have lower values for both. 5 The ears of moths have in fact evolved independently several times, making them an interesting case of convergent evolution as well. 6 Rods and cones are specialised photoreceptor cells situated in the retina of the mammalian eye and are involved in dim-light and bright-light vision, respectively. 7 Although many species from mainland Africa remain to be described, it is unlikely that the diversity of Miniopterus there will rival that in Madagascar. 8 On the kind of human family tree we usually encounter, each node represents a different individual human, with those individuals who share a more recent common ancestor, such as a father, being more closely related than those who share a more distant common ancestor, such as a great-grandfather. In a phylogeny, where each node represents a species, the same principle applies. 9 Niche modelling or SDM is, in fact, a set of many different techniques, each employing a different method. The team used Maxent (or Maximum Entropy) for the Malagasy Miniopterus study. 10 A few species, including impala and nyala, can switch between grazing and browsing as conditions change. 11 To demonstrate that the ratio of surface area to volume ratio decreases as the size of the object increases, you could perform an experiment: calculate the surface area and

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volume for three cubes with varying dimensions of 1 × 1 × 1 cm; 10 × 10 × 10 cm; and 100 × 100 × 100 cm. Strictly speaking, we should be comparing energy intake rather than food. Not all foods are ‘equal’ since they vary in energy content. The obvious exceptions are blue wildebeest and plains zebra, which routinely graze in each other’s company; this has been made possible by niche segregation with wildebeest spending longer periods in smaller patches and grazing them down, whereas zebra forage over larger spaces in search of longer grasses (Owen-Smith et al. 2015). The topi is considered conspecific with the tsessebe, Damaliscus lunatus lunatus, with the former referring to the east African subspecies and the latter to the southern Africa subspecies; but see Groves and Grubb (2011), who argue the case for us to consider them as separate species. Stable isotope analysis is done on a mass spectrometer, which separates different isotopes on their mass-to-charge ratio. The mass spectrometer actually consists of three parts: an ion source, a mass analyser and a detector. It is extremely expensive to purchase and operate! Rodents and shrews, in this case. Stable isotope analysis does not require harming animals as just a small sample of hair is needed. The taxonomy of the genus Rhabdomys has recently been revised and R. pumilio as currently understood is restricted to the Northern, Western and Eastern Cape provinces of South Africa. Based on the geographical location of Codron et al.’s study, the species in the study must have been either R. dilectus or R. chakae (Ganem et al. 2020). The morphospace is the area covered by the various components of the bat community in the hypervolume that was introduced at the beginning of this chapter (see note 2).

CHAPTER 8: FLUCTUATING POPULATIONS

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The ‘K’ in K-selection refers to the carrying capacity in the Lotka-Volterra logistic equation for population growth. The ‘r’ in r-selection refers to the growth rate in the same equation. Note that it is highly unlikely that more than four vlei rat pups from a single litter will survive, because female Otomys only have two pairs of nipples, to which the pups will cling continuously for the first weeks of their life. I have used the concepts of survival and longevity as if they are interchangeable, but they refer to different (but interlinked) phenomena. Survival rate is typically reported as the proportion of a cohort that survives a specified period of time (for example, a year), whereas longevity refers to how long individuals live. Generally speaking, high survival rates translate into longer longevities. In German and Afrikaans, the common name for a bat is in fact a flying mouse (Fledermaus and vlermuis, respectively). The terms ‘bottom up’ and ‘top down’ refer to trophic levels or positions in the food chain. Plants, which form the food of wildebeest, are at a lower trophic level, whereas lions that eat wildebeest are at a higher level compared to wildebeest. Therefore, if food regulates the wildebeest population, it is a bottom-up effect.

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CHAPTER 9: THE HUMAN FACTOR

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For example, the Triassic, which came immediately before the Jurassic, was similar in length to the Jurassic, lasting about 51 million years, from 252 to 201 million years ago; but the Cretaceous ran for almost twice as long, from 145 to 66 million years ago. The terminology that names geological ages is based on a simple system. ‘Eras’ are subdivided into ‘periods’, which in turn are divided into ‘epochs’. We currently exist in the Holocene Epoch (starting 11 000 years ago), within the Quaternary Period (starting 2.6 million years ago), within the Cenozoic Era (starting 66 million years ago). The Pleistocene Epoch, also within the Quaternary Period, started at the beginning of this period and ended when the Holocene began. Hence, the system is hierarchical in the same way that weeks and months divide the year. These five mass extinctions took place at the ends of the Ordovician, Devonian, Permian, Triassic and Cretaceous periods. It is true that wolves have been increasing their range in certain areas, such as parts of northern Europe, but in terms of ecological functioning, they are effectively extinct across much of their distributional range. The same applies to tigers, which frequently wander between protected areas in India. A primary host of the plague bacterium is the great gerbil Rhombomys opimus – a 200-gram rat-like rodent with large hindfeet and a small bushy tuft at the end of its tail – that leads a social lifestyle in the deserts of central Asia but does not occur in Europe. Swaziland officially changed its name to Eswatini in April 2018. I do not intend any disrespect to social scientists here. We did conduct some questionnaire surveys requiring us to learn and apply some very basic social research skills, but even with the best will in the world, we can hardly call this social research. The typical break-back or ‘kill’ trap has a metal or wooden base with a loop of wire attached to a strong spring. The wire is pulled back and held by a treadle that is in turn connected to a baited trigger. When the rodent touches the trigger, the loop is released and springs closed over the neck or back of the rodent, killing it. From such camera trap studies it is not only possible to determine what species are present in an area – no easy task for the more elusive mammal species – but also allows one to calculate relative abundances. Recent studies suggest that it might even be possible to calculate absolute densities of mammals detected by camera traps (Rowcliffe et al. 2008). The brown rat, thankfully, has a rather limited distribution in Africa, being mostly restricted to a few port cities, and is absent from Eswatini for now. In contrast to zoology and botany, viral families (as well as viral orders) are italicised. Measles and mumps are better-known examples of viruses from the family Paramyxoviridae, but neither of these two diseases is a zoonosis. Fortunately, human cases of henipavirus appear to be rare in Africa; but this should not lull us into a false sense of security as we should by now know how easily a pandemic can arise. There are a handful of established cases of patients with rabies who have survived, but, without the vaccine, one’s chances of survival are negligible, especially considering that some 59 000 humans die of this disease annually. In contrast, the vaccine effectively protects against the disease, as long as it is administered before the first sign of symptoms (which can take days to weeks or even months to appear).

Notes

15 A rather severe and unfortunate case of persecution of bats at the hands of local communities is the case of Rousettus aegyptiacus in Uganda. An estimated 40 000–100 000 of these fruit bats roosted at Kitaka mine, where four miners contracted the Marburg virus, one succumbing to the disease. The miners then blocked the entrance of the mine, effectively killing tens of thousands of bats, and successfully evicting the colony from the mine. The unfortunate consequence of this was the tripling of prevalence of Marburg virus in remaining populations (from around 5 per cent to more than 13 per cent) in that region of Uganda (Amman et al. 2014), putting other people at risk of contracting this deadly disease.

CHAPTER 10: THE SINKING ARK?

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In the 1980s, may I remind you, the internet did not exist. If you wanted to read a scientific article, you had to physically go to a university library and page through journals, one at a time. 2 See https://kavangozambezi.org/en/about/about-kaza, accessed 16 July 2022. 3 I should perhaps also have discussed trophy hunting here, but I find that the proponents of this debate are so fiery that it is not possible to make headway on this issue. I am personally not interested in shooting a trophy animal, but I do see the potentially enormous benefits of effectively managed hunting safaris to the empowerment of local communities and the conservation of rare and endangered species and their habitats. 4 The difficulty in defining ‘ecotourism’ is compounded by loose semantics. The prefix ‘eco-’ has today become a means to market any product, from tourism to washing powder, trading on the often unsubstantiated suggestion that it is environmentally sustainable. ‘Ecotourism’ is now routinely used in the travel industry to describe any interaction with nature, even if the operator selling the experience pursues unsustainable practices. It is thus often rendered meaningless. 5 See https://ieeexplore.ieee.org/abstract/document/5577073, accessed 16 July 2022. 6 A meta-analysis is a type of statistical analysis that attempts to answer a particular question by reviewing the literature and determining what existing studies show. For example, in the study by Krüger (2005), he compiled 251 individual case studies from which he could calculate the percentage of studies that, inter alia, demonstrated ecological sustainability. 7 Marijuana or dagga is derived from extracts of the plant genus Cannabis. 8 Someone from Eswatini is called a ‘Liswati’, plural ‘Emaswati’. 9 The ligwalagwala is the purple-crested turaco (Tauraco porphyreolophus) and is the national bird of Eswatini. The red flight feathers are worn only by the king, currently Mswati III, and members of the royal family.

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F

or those who wish to delve deeper into the topics explored in this book, I have listed below, by chapter, some key publications. These are books or review articles that relate to specific fields of study, and I have tried not to repeat the publications already cited in the body of the book. In addition, I provide names of people who have published widely in a particular relevant field – though I either do not cite their publications or I give just a single example as an illustration. If you are interested, I recommend you search for these authors online using an appropriate search engine such as Google Scholar. CHAPTER 1: A CONTINENT OF PLENTY

The beautifully illustrated six-volume Mammals of Africa is a must for any serious student or researcher of African mammalogy (Kingdon et al. 2013). Not only does it present detailed species accounts for each species recognised at the time of publication; it also has detailed overviews of each genus, family and order. Furthermore, the first volume provides a comprehensive introduction to African mammals, their evolution and basic ecology. Much of the general information presented in this chapter comes from these volumes. Additional information on the bats of Madagascar can be found in the book Les Chauves-Souris de Madagascar (Goodman 2011), but you will need to read it in French. Comparative statistics on the numbers of mammals recorded in different zoogeographic zones, which to a large extent follow continental borders, have been recently compiled by Connor Burgin and co-authors (Burgin et al. 2018). This in turn is based on the Mammal Diversity Database (https://mammalodiversity. org), a regularly updated and publicly accessible website, curated by a group of

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40  world-renowned mammalogists, which I highly recommend for anyone interested in the latest taxonomic listing of the world’s mammals. For bats and bat taxonomy, I highly recommend the website https://batnames.org, managed and regularly updated by Nancy Simmons and Andrea Cirranello (Simmons and Cirranello 2020). CHAPTER 2: THE SPECIES CONUNDRUM

The celebrated zoologist and evolutionary biologist Ernest Mayr lived to be 100 years old, and published papers and books over a period of 80 years. His book Systematics and the Origin of Species, first published in 1942 (Mayr 1942), is still relevant today and provides an interesting historical background to modern thought on systematics. In this book, Mayr clearly outlines the biological species concept. A review of species concepts and how they have been applied to African mammals can be found in ‘Species Definitions and Conservation: A  Review and Case Studies from African Mammals’ by Colin Groves et al. (2017), who argue convincingly for the phylogenetic species concept. Species concepts are fundamental to conservation, because the way we view what a species is will affect how we identify and distinguish species on the ground, leading to lumping and/or splitting. For a contrary view see ‘Species Inflation and Taxonomic Artefacts: A Critical Comment on Recent Trends in Mammalian Classification’ by Frank E. Zachos et al. (2013). I am not aware of a book or review that provides a comprehensive overview of the speciation of African mammals. However, great strides have been made in understanding the biogeographic processes affecting speciation in certain groups of mammals. For example, Josef Bryja, of the Czech Academy of Sciences, and his team of students and collaborators have published recent and detailed reviews of the systematics and probable routes of speciation for many rodent genera within the family Muridae; see, for example, ‘Phylogenomics of African Radiation of Praomyini (Muridae: Murinae) Rodents: First Fully Resolved Phylogeny, Evolutionary History and Delimitation of Extant Genera’ (Nicolas et al. 2021). One cannot talk about rodent systematics in Africa without mentioning Violaine Nicolas and Christiane Denys, both from the Muséum National d’Histoire Naturelle in Paris, France, who together with Josef Bryja are among the most prolific systematists working on African small mammals. Another prolific group hails from the Field Museum in Chicago, USA, and

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includes Steve Goodman, Bruce Patterson, Julian Kerbis Peterhans and Terry Demos; for example, see ‘Evolutionary Relationships and Population Genetics of the Afrotropical Leaf-Nosed Bats (Chiroptera, Hipposideridae)’ (Patterson et  al. 2020). Other dominant figures include Peter Taylor, of the University of the Free State, South Africa, whose systematic work on Otomys I used to illustrate biogeographic principles in chapter 5, and Rainer Hutterer, of the Zoological Research Museum Alexander Koenig in Bonn, Germany, the doyen of shrew taxonomy. A quick Google Scholar search for any of these names will offer easy entry into the relatively unknown world of the taxonomy of African small mammals. CHAPTER 3: THE HISTORY OF AFRICA’S MAMMALS

Two excellent texts serve as entry points for those interested in extinct African mammals: the six-volume Mammals of Africa (Kingdon et al. 2013), and Cenozoic Mammals of Africa (Werdelin and Sanders 2010), although the latter is restricted to the past 66 million years. Jennifer Botha-Brink, of the National Museum in Bloemfontein, South Africa, seems to be involved with any study dealing with therapsids (and many other taxa) from Karoo sediments in South Africa, with an impressive list of publications; see, for example, ‘Biostratigraphy of the Lystrosaurus Declivis Assemblage Zone (Beaufort Group, Karoo Supergroup), South Africa’ (Botha and Smith 2020). An alternative, and mostly refreshing, discussion on alien invasive species is Ken Thompson’s book Where Do Camels Belong? (Thompson 2015). CHAPTER 4: ISLANDS AS SPECIES FACTORIES

Natural History of Madagascar, consisting of more than 1 700 pages, comprehensively covers everything that was known about Malagasy plants and animals at the time of its publication (Goodman and Benstead 2003). A fully revised version of this book is due to be published in 2022 (Goodman 2022). Nearly every paper on the bats, rodents and tenrecs of Madagascar has Steve Goodman’s name somewhere in its list of authors. In addition to the book on the bats of Madagascar cited in chapter 1, Goodman has also published books on terrestrial small mammals, carnivores, and recently extinct mammals (Goodman 2012; Goodman and Jungers 2013; Soarimalala and Goodman 2011), all written in

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French. All you would like to know about the lemurs of Madagascar has been published in a fully illustrated book, Lemurs of Madagascar (Mittermeier et al. 2010). CHAPTER 5: EVOLUTION ON THE MAINLAND

Another beautiful book by Jonathan Kingdon is Island Africa: The Evolution of Africa’s Rare Animals and Plants (1989). This provides an insightful look at how organisms have evolved on the continent. As usual, much useful and interesting information can be gleaned from Mammals of Africa (Kingdon et al. 2013). Thomas Couvreur and his co-authors have published an excellent and recent review of how climate and plate tectonics have affected speciation of plants and animals in Africa, ‘Tectonics, Climate and the Diversification of the Tropical African Terrestrial Flora and Fauna’ (Couvreur et al. 2021). Jean Maley has published extensively on the contraction and fragmentation of African rainforests; a recent example of this work is ‘Late Holocene Forest Contraction and Fragmentation in Central Africa’ (Maley et al. 2018). Peter Taylor has published extensively on the systematics and taxonomy of one group of Afromontane specialists, the vlei rats of the genus Otomys. For a recent example, see ‘Biomes, Geology and Past Climate Drive Speciation of Laminate-Toothed Rats on South African Mountains (Murinae: Otomys)’ (Taylor et al. 2019). CHAPTER 6: GIANT MAMMALS SHAPING THE LANDSCAPE

Norman Owen-Smith’s 1987 article ‘Pleistocene Extinctions: The Pivotal Role of Megaherbivores’ is a good starting point (Owen‐Smith 1987). The journal Proceedings of the National Academy of Sciences of the United States of America published a special feature titled ‘Megafauna and Ecosystem Function: From the Pleistocene to the Anthropocene’ in 2016 (vol. 113, no. 4) that included ten interesting and related papers. I highly recommend these papers as further reading on this topic. Other papers on this topic relevant to Africa include ‘Ecosystem-Scale Effects of Megafauna in African Savannas’, (Asner et al. 2016), ‘The African Rainforest: Odd Man Out or Megafaunal Landscape? African and Amazonian Forests Compared’ (Terborgh et al. 2016), and ‘A Refined Chronology of Prehistoric Madagascar and the Demise of the Megafauna’ (Crowley 2010).

282

Recommended Reading

Unsurprisingly, many books have been published on the functioning of ecosystems in the Serengeti and Kruger National Park landscapes. The most recent in the Serengeti series is Serengeti IV: Sustaining Biodiversity in a Coupled Human-Natural System and covers 832 pages (Sinclair et al. 2015). The Kruger Experience was published a decade earlier (Du Toit et al. 2003), and brings together the contributions of more than 100 scientists who have conducted research in this ecosystem. Both these books are amazing contributions to their field and well worth reading. Ross MacPhee’s recent book End of the Megafauna: The Fate of the World’s Hugest, Fiercest, and Strangest (MacPhee 2018) provides an engaging overview of the late Pleistocene extinctions and presents evidence for the opposing arguments that have been previously articulated, including the role of humans. CHAPTER 7: A PLACE FOR EVERY SPECIES

James Lovelock, who died on 26 July 2022 (aged 103), first published Gaia: A New Look at Life on Earth in 1979. This is a must-read for anyone interested in planet Earth (Lovelock 1979), even if its central thesis that the Earth functions as a single super-organism is untenable and probably now discredited. Evelyn Hutchinson’s paper on the niche, ‘Homage to Santa Rosalia or Why Are There So Many Kinds of Animals?’ (Hutchinson 1959) is still worth reading. I am not aware of any comprehensive review of the community ecology of African large mammals since the publication of Walter Leuthold’s 1977 book, African Ungulates: A Comparative Review of Their Ethology and Behaviour (Leuthold 1977). Many books have been written on the plains antelopes of Africa, but I am not aware of a recent book that covers the ecology of a community, as opposed to field guides or books that deal with just a single species. Richard Estes’s highly readable and informative but dated book, The Behaviour Guide to African Mammals (Estes 1991), comes close, and is another must-read for anyone interested in African mammals. The seminal, and lengthy, paper by P.J. Jarman, ‘The Social Organisation of Antelope in Relation to Their Ecology’ is still essential reading for anyone interested in the social organisation of African antelope (Jarman 1974), as is the shorter, yet equally seminal, contribution of Richard Bell, ‘A Grazing Ecosystem in the Serengeti’ (Bell 1971).

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Look out for the more than 200 scientific papers that Norman OwenSmith, of the University of the Witwatersrand, South Africa, has published on ungulates, and for works by the multitude of students he has guided and mentored over the years, such as Johan du Toit, of Utah State University, USA (and former director of the Mammal Research Institute, University of Pretoria, South Africa), and Joseph Ogutu, of the University of Hohenheim, Germany. Tony Sinclair, of the University of British Columbia, Canada, has been similarly influential, with a focus on the Serengeti ecosystem. One of the first publications to test the general applicability of stable isotopes to studying African mammal communities was ‘The Isotopic Ecology of East African Mammals’ (Ambrose and DeNiro 1986). CHAPTER 8: FLUCTUATING POPULATIONS

Life history and demographic information on individual species of African small mammals can be obtained from Mammals of Africa Vol. IV: Hedgehogs, Shrews and Bats (Happold and Happold 2013), and Bats of Southern and Central Africa: A Biogeographic and Taxonomic Synthesis (Monadjem, Taylor et  al. 2020). Two useful but dated publications, ‘The Ecology of Small Rodents in Tropical Africa’ and ‘Ecology of Small Rodents in Africa’ (Delany 1972, 1986) provide a review of this topic for terrestrial small mammals. Mike Perrin made valuable contributions to this field over a three-decade period and trained up many of the current stock of small mammal ecologists (he supervised my PhD). A useful synthesis of the demographic (reproductive) parameters of African rodents is found in ‘Reproductive Response of Tatera leucogaster (Rodentia) to Supplemental Food and 6-Methoxybenzoxazolinone in Zimbabwe’ (Neal 1996). If you are interested in methods for studying small mammals, then the following two books are essential: Ecological and Behavioral Methods for the Study of Bats (Kunz and Parsons 2009), and Methods for Ecological Research on Terrestrial Small Mammals (McCleery et al. 2021) for non-volant small mammals such as rodents and shrews. PhD theses are rarely published as is; an exception is that of Herwig Leirs, titled Population Ecology of Mastomys natalensis (Smith, 1834): Implications for Rodent Control in Africa (Leirs and Verheyen 1995), which remains a remarkable contribution to this field and well worth getting a copy of.

284

Recommended Reading

The Pest Management Centre, Sokoine University of Agriculture, Tanzania, has been at the forefront of research on African pest rodents. Rhodes Makundi, Apia Massawe and Loth Mulungu have been involved with an impressive array of studies across the region; they have trained dozens of postgraduate students in this field and have produced important reviews, including ‘Ecologically Based Rodent Management in Africa: Potential and Challenges’ (Makundi and Massawe 2011). CHAPTER 9: THE HUMAN FACTOR

For an overview of the Anthropocene, as relevant to bats, see Bats in the Anthropocene: Conservation of Bats in a Changing World (Voigt and Kingston 2016); this edited book contains an impressive range of chapters, authored by the world’s top bat biologists. In the present book, I have purposefully avoided discussing human-wildlife conflict in the context of large and dangerous mammals such as elephants and lions. There are hundreds of papers on this topic and several good books, such as People and Wildlife: Conflict or Co-Existence (Woodroffe et al. 2005). The field of ecosystem services has exploded onto the scene in the past decade or so. In fact, it is now difficult to get funding for ecological research if the term ‘ecosystem services’ does not appear prominently somewhere in the grant. I guess this is our last-ditch effort at demonstrating the economic importance of retaining wild plant and animal populations, in order that society prioritises the conservation of biodiversity. Plenty of studies across the globe have been published on the ecosystem services provided by mammals (and many other organisms), but much of this work has been conducted outside of Africa. The numerous ecosystem functions performed by mammals have been comprehensively reviewed by T.E. Lacher et al. (2019). See ‘Bird and Bat Predation Services in Tropical Forests and Agroforestry Landscapes’ (Maas et al. 2016) for a review of ecosystem services provided by bats and birds in tropical regions of the world. I have already aired in detail the great contributions made by Peter Taylor, his students and collaborators. For a brief discussion of what we know about animal ecology in African urban environments, see ‘Urban Animal Diversity in the Global South’ (Reynolds et al. 2021).

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An excellent, albeit rather dated, book pertaining to zoonoses and their spillover into human society, written for the layperson, is Spillover: Animal Infections and the Next Human Pandemic (Quammen 2012), which is still well worth a read for a broad overview of the subject. For more information on batborne diseases in Africa, look for Wanda Markotter’s many publications. CHAPTER 10: THE SINKING ARK?

The International Union for Conservation of Nature (IUCN) red list of threatened species (https://www.iucnredlist.org) is an excellent, and free, online resource for obtaining information on the conservation status of any African mammal (or indeed any vertebrate species in the world). Although now out of date, the paper by J. Schipper et al. (2008), ‘The Status of the World’s Land and Marine Mammals: Diversity, Threat, and Knowledge’, provides a useful overview of what we know about threats to mammals across the globe. An excellent book on how (and why) to meaningfully involve communities in conservation activities in Africa is An Arid Eden: A Personal Account of Conservation in the Kaokoveld by Garth Owen-Smith, the brother of Norman Owen-Smith (Owen-Smith 2010). Another useful book dealing with many aspects of conservation is Institutional Arrangements for Conservation, Development and Tourism in Eastern and Southern Africa: A Dynamic Perspective (Van der Duim et al. 2015); chapter 9 of this book is dedicated to transfrontier conservation areas in southern Africa and well worth reading. For more information on Eswatini, refer to Mike Unwin’s travel guide, Swaziland (Unwin 2012). Although Eswatini is often included in red list books published by South Africa, it has also produced its own, for example Threatened Vertebrates of Swaziland, Swaziland Red Data Book: Fishes, Amphibians, Reptiles, Birds and Mammals (Monadjem et al. 2003). A history of conservation action in Eswatini is presented in The Mlilwane Story: A History of Nature Conservation in the Kingdom of Swaziland and Fund Raising Appeal (Reilly 1985) and The Lion Roars Again: A Reflection on the History and Significance of Hlane Royal National Park and Other Conservation Achievements of the Monarchy in the Kingdom of Swaziland (Reilly and Reilly 1994); however, note that neither of these two publications is readily available.

286

INDEX

A aardvark (Orycteropus afer) 14, 69–70 Accipiter melanoleucus (black sparrowhawk) 76 Acinonyx jubatus see cheetah Acontias 34 addax (Addax nasomaculatus) 28–29, 123 Aepyornithidae (ratites) 136 Aethomys (veld rats) 173 Afar Triple Junction 103 Africa and islands map 7 fig 1.1 African ecosystems 22–36, 23 fig 1.6 African harrier-hawk (Polyboroides typus) 20 African islands 80–82 African palm (Hyphaene petersiana) 142 African wild dog (Lycaon pictus) 157, 226 African wildcat (Felis lybica) 208 Afromontane ecosystem 30 realm: mountains as ‘islands’ 120–124 region of South Africa 30 Afrotheria 14, 67–73, 92, 126 Afrotropics 11–12, 13 table 1.1 Agapornis nigrigenis (black-cheeked lovebird) 30 ‘The Age of Mammals’ 56, 138 ages of rodents (knowing) 181 Agulhas current 35 Ahlquist, Jon 50 Aïr mountain 30

Albert (lake) 104 Albertine Rift 24–25, 29–30, 92, 106–107, 110–111 Albertine Rift transition zone 102–106 Aldabra Atoll 83, 84 table 4.1, 134–135 Aldabrachelys see tortoises, giant Aldabrachelys gigantea see tortoises, Aldabra Alopochen aegyptiaca (Egyptian goose) 76 Amazon Forest/Rainforests 24, 106, 282 Amazon River 116 Anabat bat detector/system 146 fig 6.9 The Ancestor’s Tale 62 Andean expedition 149 Angola 29, 30, 35, 45, 113, 116, 225–226 Anjouan 81, 84 table 4.1, 86 Annobón 82, 84–85 table 4.1, 86 anomalurids see squirrels, flying 5, 72 Antarctic Indian Ocean 82 Antarctica 35, 68–69 antelope 5, 70, 72, 102 adaptive radiation 71 cloven-hoofed 95 decline 140 grazers and browsers 160 plains 124, 156, 159–166 population regulation 186–191 water-dependent antelope 140 woodland 138 Anthropocene 192–194, 216, 285 Antidorcas marsupialis (springbuck) 224 fig 10.3 aquatic ecosystems 31, 33 fig 1.8a

AFRICAN ARK

aquatic habitats see freshwater aquatic habitats Arabia 6, 73, 103–104, 112 Arabian land crossing 73 Arabian Peninsula 103 Arabian Sea 82 Arctocephalus pusillus (Cape fur seals) 35 Argentinosaurus 125 Arthroleptella (Moss frog) 32 Arthroleptella rugosa see frogs, rough moss Arvicanthus (grass mice) 49 Astrochelys radiata 134 Atilax paludinosus (marsh mongoose) 32 Australia 3, 42, 47, 60, 68–69, 72, 75, 127, 130, 133, 148 B baboon hamadryas baboon (Papio hamadryas) 42 olive baboon (Papio anubis) 42 Bamford, Andy 21 barbet Chaplin’s (Lybius chaplini) 30 barriers 99–106 climate 124 mountains 124 rivers 124 vegetation 124 Bathyergidae (mole-rats) 173 bat-eared fox (Otocyon megalotis) 113 bats Angolan free-tailed (Mops condylurus) 17–18, 98 animalivorous 159 Brandt’s (Myotis brandtii) 185 colonisations, Madagascar 95–98 common (or Egyptian) slit-faced (Nycteris thebaica) 183, 184 fig 8.5, 185, 205 fig 9.6 community structure 152–159 Egyptian free-tailed (Tadarida aegyptiaca) 63, 64 fig 3.3 Egyptian tomb bat (Taphozous mauritianus) 88, plate 1

288

free-tailed (Molossidae) 63, 97, 154 frugivorous 159 horseshoe (family Rhinolophidae) 47–48, 54, 153 Hypsignatus monstrosus plate 1 insectivorous free-tailed (Mormopterus) 88 little free-tailed (Chaerephon pumilus) 17–18 long-fingered (genus Miniopterus) 95–96, 157–159 Macronycteris vittatus plate 1 Malagasy (Madagascar) 95, 159 Midas free-tailed (Mops midas) 97, 97 fig 4.7 Miniopterus aelleni 96 Miniopterus grivaudi 96 Miniopterus nimbae plate 1 Mops leonis plate 1 Mops leucostigma 98 Nycteris arge plate 1 omnivorous 159 Pipistrellus hesperidus 96 Rhinolophus 47, 49 Rhinolophus hillorum plate 1 Rhinolophus sakejiensis 54 Roberts’ flat-headed (Sauromys petrophilus) 63 Rüppell’s horseshoe (Rhinolophus fumigatus) 48 fig 2.4 Scotophilus nux plate 1 Taphozous mauritianus plate 1 ultimate K-selected mammals 183–186 Villiers’ long-fingered (Miniopterus villiersi ) 158 fig 7.4 Beaufort Group 59, 281 Bell, Richard 160, 283 Belmain, Steve 197, 199 fig 9.4 Benguela current 35 Benin 107, 166 Big Game Parks (Eswatini) 234 biodiversity hotspots see hotspots biogeography 45, 100 ‘theory of island biogeography’ 80, 87, 221

Index

Bioko 82, 86–87 Biological Conservation 218 biological diversity 1, 29, 231 biological species concept 280 black-cheeked lovebird (Agapornis nigrigenis) 30 Black Death (Yersinia pestis) 195 black mamba (Dendroaspis polylepis) 39 black-shouldered kite (Elanus caeruleus) 180, 204 black sparrowhawk (Accipiter melanoleucus) 76 black wildebeest (Connochaetes gnou) 13 blue antelope (Hippotragus leucophaeus) 100, 123–124 blue wildebeest (Connochaetes taurinus) 13, 162, 187, 188 fig 8.6, plates 10–12 Bohmann, Kristine 17–18, 17 fig 1.4 Bond, William 136 Bostrychia hagedash (hadeda ibis) 76–77 Botswana 5, 113, 116, 139, 182, 224–226 Bowie, Rauri 120 Brachyuromys 91 buffalo 28, 140, 160–163, 172 fig 8.1, 189 African buffalo (Syncerus caffer) 161 fig 7.5b, 166, 186, 226 Cape buffalo (Syncerus caffer) 171–172 Burgin, Connor 11, 279 Burundi 29, 104 bushpig (Potamochoerus larvatus) 102 Butchart, Duncan 20 Butynski, Thomas 9 Bwindi Impenetrable Forest 26 fig 1.7b Bwindi Impenetrable National Park 37, 221 Byrom, Andrea 180 C Cameroon 25, 29, 107, 110 Mount Cameroon 82 Cameroon-Nigeria Highlands 111 Cameroon Volcanic Line 82

CAMPFIRE see Communal Areas Management Programme for Indigenous Resources Canary Islands 6, 82–83, 249 Canis mesomelas see jackals, blackbacked Cape buffalo (Syncerus caffer) 171–172 Cape Cross, Namibia 35 Cape Fold Mountains 32, 52 Cape region, South Africa 25 Carruthers, Vincent 32 Cathartes aura see vultures, turkey Central African Republic 116 Ceratotherium simum see rhinoceroses, white cetacean species 35 Chad 28–29, 182 Chaerephon pumilus (little free-tailed bat) 17–18 Chambeshi River 116 Channing, Alan 34, 52 cheetah (Acinonyx jubatus) 12, 156–157, 226, plate 15 chimpanzee 110, 117–118 bonobo/pygmy (Pan paniscus) 117–118 common (Pan troglodytes) 117–118, plate 14 central 118 eastern 118 Elliot’s/Nigerian 118 distribution 117 fig 5.7 Chlorocebus aethiops (vervet monkeys) 38 Chobe National Park 226 Choeropsis liberiensis (pygmy hippopotamus) 31 Clements, Frederic 150, 169 cobra see spitting cobra Codron, Jacqueline 167 coevolution 155–157 Collier, Bret 185 Communal Areas Management Programme for Indigenous Resources (CAMPFIRE) 231, 234 community ecology 149, 152, 283

289

AFRICAN ARK

Comoé National Park 25 Comoros 6, 81, 84 table 4.1, 85–86, 88, 91, 96, 98 competitive exclusion principle 152 Congo Basin 24–25, 32, 44, 100, 105, 109, 111, 116, 119–120, 124 map 103 fig 5.2 Congo Republic 107, 110 Congo River 24, 100, 110, 116–117, 119–120 map 103 fig 5.2 Connochaetes gnou (black wildebeest) 13 Connochaetes taurinus see blue wildebeest conservation and community development 219–221 and ecotourism 227–229 and management of protected areas 221–225 Conservation Biology 218 conservationists and ecologists 217–219 coral atolls/reef 5, 82 Coronaviridae 210, 212 coronaviruses in bats 214 Cotterill, Woody 9, 54, 121 COVID-19 210, 212–213, 225, 236 Cretaceous Period 65, 67, 193 Cretaceous Terrestrial Revolution 67 Cricetomys (giant rats) 90 Crick, Francis 46 Crocidura canariensis (insectivorous shrew) 83 Crocidura genus see shrew Crocidura poensis 86 Crocidura thomensis 86 Crocuta crocuta see hyena, spotted crop damage 195–196, 198 insects 204 perceived 39 post-harvest losses 198, 200 pre-harvest losses 198 rodents 180 Cylindraspis see tortoises, giant Cynictis penicillata (yellow mongoose) 206 fig 9.7 cynodonts 61–62, 65

290

D dagga/marijuana cultivation 234 Dahomey Gap 107, 118 Damaliscus lunatus see tsessebe Damaliscus lunatus jimela see topi Darwin, Charles 49, 79 dassies see hyraxes Dasymys (marsh rats) 10 Dawkins, Richard 62 Deinotherium 2, 56, 57 fig 3.1, 126 Democratic Republic of the Congo (DRC) 29, 104, 107, 116, 212 Demos, Terry 106, 281 Dendroaspis polylepis (black mamba) 39 Dendrohyrax 70 Dendrohyrax arboreus (southern tree hyrax) 102 Dendrohyrax dorsalis (western tree hyrax) 102 Dendromus see mice, climbing Denys, Christiane 9, 121, 280 Dermochelys coriacea (leatherback turtle) 62 Diceros bicornis see rhinoceroses, black dik-dik (Madoqua kirki) 113, 160, 161 fig 7.5a Dimetrodon 58 Dinornithiformes (moas) 136 Diprotodon (marsupials) 3, 126 Dlamini, Nomfundo 199 DNA 18, 46–47, 55, 89, 158, 164 DNA-DNA hybridisation 50 dolphin 35 dormice (Gliridae) 173 DRC see Democratic Republic of the Congo duikers 28, 138, 160, 162, 166 Duvenhage bat lyssavirus 213 E eagles 38 crowned (Stephanoaetus coronatus) 39 fish 139 martial (Polemaetus bellicosus) 39 Eastern Arc forests 105

Index

Eastern Arc Mountains 102, 223 Eastern Cape, South Africa 8, 25, 59 Eastern Rift 103–106 eastern rift valley 29 Ebola 210, 212 echidna (Tachyglossidae) 60, 63 echolocation 16, 154–155, 155 fig 7.2, 159 ecologists and conservationists 217–219 ECORAT 198–199 EcoRodMan 199 ecosystem services xxi, 2, 14–17, 32, 36, 139 fig 6.6, 145, 192, 201, 209, 285 by bats 204 by mammals 202 table 9.1, 216, 285 by rodents 201–205 ecotourism 227–232, 230 fig 10.5 and conservation 227–229 Edward (lake) 104 Eger, Judith L. 9 Egyptian fruit bat (Rousettus aegyptiacus) 212 Egyptian goose (Alopochen aegyptiaca) 76 eland 162 Taurotragus derbianus (giant eland) 70 Taurotragus oryx 190 Tragelaphus oryx 140 Elanus caeruleus see black-shouldered kite Elapidae (cobras and mambas) 51 Eldana (moths) 18 elephant African (Loxodonta) 127 forest (Loxodonta cyclotis) 15, 102 Indian (Elephas) 127 paradox 141–147 savanna (Loxodonta africana) 15–16, 102, 125–127, 141, 146 fig 6.9, 226, plate 9 elephant bird (ratites) 136 Elephas (Indian elephant) 127 Elgon (mountain) 122 Elliot’s chimpanzee 118

Elton, Charles 150–151 ‘Eltonian’ niche(s) 151–152, 154, 157–159, 169 emigration 170, 176–177 end-Cretaceous event/mass extinction 65–66, 125 end-Permian event/mass extinction 60–61, 193 Eocene 74 table 3.2 Eocene Epoch 58 table 3.1, 73 epochs (geolocical) 58, 58 table 3.1, 74–75 table 3.2, 192, 216 Equus burchelli see zebra eras (geological) 58, 58 table 3.1 Eswatini (Swaziland) 17, 30, 77, 143– 147, 180, 197 fig 9.3, 202–203, 207–208, 214 conservation 232–239, 286 community-based 235–239 population 225 populations of rodents 180, 185 protected areas 233 fig 10.6 Eswatini Nation Land (ENL) 234 Eswatini National Trust Commission 234 Ethiopia 28–30, 102–104, 113, 120 highlands 5, 123 Eudorcas thomsonii (Thomson’s gazelles) 164 Eurasia 2–3, 6, 56, 69–70, 72–73, 74–75 table 3.2, 93, 123, 127, 130, 133, 148 Eurasian mammals 77 evolution xxi–xxii, 42–47, 47–50, 62 Charles Darwin’s theory 79 coevolution 155–157 evolutionary time 77, 154 history 70 of mammals 55, 67 in microcosm (Madagascar) 88–98 lineages across evolutionary time 47–50 mammalian 59, 65, 81 of a continent 1–3 on African Mainland 99–124

291

AFRICAN ARK

F facilitation (concept) 163 Felis lybica (African wildcat) 208 Fiedler, Lynnwood 182 Filoviridae 210, 212 fish 31–32, 116, 139–140 fluctuating populations 170 flying foxes (Pteropus species) 86, 88 lesser Mascarene flying fox (Pteropus subniger) 88 forests and deserts 24–29 fossils 50, 62 bats 49 cynodont 61, 65 Karoo 57, 59 mammal 56 fox, bat-eared (Otocyon megalotis) 113 Franklin, Rosalind 46 Free State 59 freshwater aquatic habitats 29, 31–32 role of hippopotamuses 140 frogs 79, 92 Anura 52 moss (Arthroleptella) 32 rough moss (Arthroleptella rugosa) 52, 53 fig 2.5 function or form 37–40 functional diversity 14–22 functional species concept 39 fynbos 25, 29, 32–34, 153, 202 fynbos ecosystems 33 fig 1.8c G Gabon 25, 107, 110 Gaia hypothesis 150 gemsbok (Oryx gazella) 113 ‘General Vertebrate Model’ hypothesis 158 genets 42, 180, 206–207 aquatic (Genetta piscivore) 32 Genetta piscivore (aquatic genet) 32 Geogale auritus (large-eared tenrec) 92 geological landscape changes 43–45 Gerbilliscus see gerbils gerbils (Gerbilliscus) 91, 173

292

Ghana 24, 107 Gilbert, Tom 18 Giraffa camelopardalis see giraffes giraffes (Giraffa camelopardalis) 126–127, 128–129 fig 6.1d, 189 glacial 44–45, 109, 113–114 events 132, 132 fig 6.3 Gleason, Henry 150, 169 Gliridae (dormice) 173 Gondwana 68, 72, 80–82 Goodman, Steve 9, 54, 95, 96 fig 4.6, 157, 281 Gorilla beringei beringei (mountain gorillas) 38 fig 2.1 Gorilla gorilla (western gorillas) 110 Gorillas (genus Gorilla) 37–38, 110–111, 111 fig 5.5, 117 mountain gorillas (Gorilla beringei beringei) 38 fig 2.1 western gorillas (Gorilla gorilla) 110 Gorongosa National Park 25, 145 fig 6.8 Grande Comore 81, 84 table 4.1 Great American Interchange 77 Great Limpopo Transfrontier Park 187 Great Rift Valley 24, 103–104 map 103 fig 5.2 Gregory Rift (Eastern Rift or Rift Valley) 103–104 Grinnell, Joseph 150–151 ‘Grinnellian’ niche(s) 151–152, 157–159, 169 Guinea (rain) forests Lower 25, 105, 107, 111 Upper 24, 31, 105, 107, 109, 118 Guinean savannas 191 Gulf of Aden 103 Gulf of Guinea 6, 82–83, 86, 91 islands 84–85 table 4.1, 86, 87 fig 4.2 Gumbi, Charles 143 fig 6.7 Gyps africanus see vultures, African white-backed Gyps coprotheres (Cape vulture) 21 Gyps vultures 20

Index

H ‘Habitat First Rule’ hypothesis 157, 159 hadeda ibis (Bostrychia hagedash) 76–77 Hansen, Anders 214 Happold, David 9 Happold, Meredith 9 harrier-hawk (Polyboroides typus) 20 Heliosciurus gambianus (Gambian sun squirrel) 104 Heliosciurus mutabilis (mutable sun squirrel) 102 Heliosciurus rufobrachium (red-legged sun squirrel) 102 Helogale parvula (dwarf mongoose) plate 8 Hendra virus 213 Henipavirus (Paramyxoviridae) 213 Heterohyrax 70 Heterohyrax brucei see hyraxes, yellow-spotted Himalayas 44 hippopotamus(es) 2, 31–32, 36, 126–127, 128–129 fig 6.1c, 136, 139–140, 162 common (Hippopotamus amphibius) 31, 135–136 pygmy (Choeropsis liberiensis) 31 Hippopotamus amphibius see hippopotamus, common Hipposideridae 48–49, 281 Hippotragini tribe 123 Hippotragus equinus see roan antelope Hippotragus leucophaeus see blue antelope Hippotragus niger see sable antelope Hlane Royal National Park 146–147, 233 fig 10.6, 234 Hoffmann, Michael 9 Hoggar mountain 30 Holocene epoch 58 table 3.1, 193 Homo sapiens 3, 133 extreme domination 131 devastation 132 disappearance of animals 132 super predator 130, 147

hotspots (biodiversity) 25, 103, 106–108 for bats 168 human factor 192–216 human-animal conflict 209 human-wildlife conflict 194, 227, 285 human-wildlife interactions 216 humans and small mammals – negatives 194–201 and small mammals – positives 201–209 Hutchinson, Evelyn 151–152, 283 Hwange National Park 226, 231 Hyaena brunnea (brown hyena) 35 Hydrophiinae subfamily (sea snakes) 62–63 hyena 19, 21, 28 brown (Hyaena brunnea) 35 spotted (Crocuta crocuta) 157, 226, plate 16 Hylomyscus denniae 106 Hylomyscus kerbispeterhansi 106 Hylomyscus simus see mice, wood Hyphaene petersiana (African palm) 142 Hypogeomys antimena (giant jumping rat) 91, 91 fig 4.4 Hypsignatus monstrosus plate 1 hyracoids 71, 95 hyraxes (dassies) 69–70 southern tree (Dendrohyrax arboreus) 102 western tree (Dendrohyrax dorsalis) 102 yellow-spotted (Heterohyrax brucei) 71 (fig 3.5), plate 7 Hystricidae (porcupines) 173 I immigration 88, 170, 176–177 India 22, 68, 82, 88 tectonic plate 44 Indian Ocean 35, 81, 116 Islands 88, 90 Indian subcontinent 88

293

AFRICAN ARK

individualistic responses of species 149–150, 169 Indomalaya 11–12, 13 fig 1.1 Indricotherium transouralicum 56 instability 44, 106 interglacial 44–45, 109, 113 International Union for Conservation of Nature (IUCN) 28–29, 286 invasions: ‘alien’ species 75–77 island mammals Africa’s 82–88 islands African 80–82 as species factories 79–98 associated with Africa 7 fig 1.1, 84–85 table 4.1 Canary 82–83 Comoros 85, 88 extinct 82 Gulf of Guinea 83, 86 Indian Ocean 90 Mahé 83 Mascarene 6, 81, 83, 84 table 4.1, 88, 91, 135 Prince Edward 82 Rodrigues 82–83, 88, 134 Seychelles 83 Tristan da Cunha 82 volcanic 81–82 Zanzibar 87 IUCN see International Union for Conservation of Nature Ivory Coast 25, 107 Iziko South African Museum, Cape Town 52 J jackals 19, 21, 69, 180 black-backed (Canis mesomelas) 35, 113, 114 fig 5.6 Jacobs, David 153–154 Jaculus deserti 112 Jaculus genus see jerboas Jaculus jaculus 112 Jaculus orientalis 112 Jarman-Bell Principle 160, 162

294

Jarman, Peter 160, 283 jerboas (genus Jaculus) 112 Jordan 212 Jurassic Period 56, 58 table 3.1, 61, 65, 67, 193 K Kafue National Park 226, 233 Kakamega Forest, Kenya 25 Kalahari Gemsbok National Park 224 Kalina, Jan 9 KaMsholo Bushveld Safaris 234 Kane, Adam 21 Karoo biomes 202 fossil deposits 57 geology 65 rock beds 57, 59 sediments 281 Karoo Supergroup 59, 281 Kartzinel, Tyler 164 Kasai river 116 Kavango-Zambezi Transfrontier Conservation Area (KAZA TFCA or KAZA) 225, 226 fig 10.4 KAZA see Kavango-Zambezi Transfrontier Conservation Area Kennis, Jan 119 Kenya 15, 25, 28, 44, 103–105, 113, 122, 164–165, 182, 187, 221–223 Mount Kenya 29, 115 Kgalagadi Transfrontier Park 224 Kilimanjaro 29, 123 Kingdon, Jonathan 9, 102, 282 Kirindy, Madagascar 136 Kisangani 119 Kivu (lake) 104 knob-thorns (Senegalia nigrescens) 144, 204 Kruger, Laurence 142–144, 145 fig 6.8 Kruger National Park, South Africa 25, 107, 140, 142, 144–147, 157, 162, 187, 189–191, 283

Index

Krüger, Oliver 228–229 Kuiseb River, Namibia 45 KwaZulu-Natal 25, 42, 59 L Lagos bat lyssavirus 213 Laos 52 Lascaux paintings 133 Last Glacial Maximum (LGM) 87, 109–111, 133 Laurasia 68, 70, 72 LAZ (Lystrosaurus Assemblage Zone) 59 leatherback turtle (Dermochelys coriacea) 62 Ledger, John 20 Leirs, Herwig 119, 180–182, 284 Lemniscomys (striped mice) 49, 173–174, 176–177, 203 Lemniscomys rosalia see mice, singlestriped grass lemurs (family Lemuridae) 89–90, 95 aye-aye (Daubentonia madagascariensis) 93 cat-sized (Propithecus) 93, 94 fig 4.5b diet on vertebrates (Mirza) 93 diurnal (Eulemur) 93 gorilla-sized (Archaeoindris) 93, 135 koala lemur (Megaladapis) 135 Madagascar 93–95 mouse-sized (Microcebus) 93 nocturnal (Lepilemur) 93 Phaner 93 ring-tailed lemur (Lemur catta) 93 sloth lemur (Palaeopropithecus) 135 tail-less (Indri indri) 93, 94 fig 4.5 leopard (Panthera pardus) 39, 156, 226 Lepus saxatilis (scrub hare) 14 Lesotho 30, 59 Levin, Simon 151 Levinsky, Irina 111 LGM see Last Glacial Maximum Liberia 25, 107 life history 171–178, 183, 191, 284 strategies 171–173, 176–177, 191 traits 171, 175 table 8.1, 176, 178, 183

Linden, Valerie 204 lineages 45–48, 50, 92, 113, 123, 183 Linnaean hierarchy 12 Linnaeus, Carl 51–52 lion (Panthera leo) 39, 50, 156, 156 fig 7.3, 226 litopterns 126 Lomani river 116 Lophuromys (brush-furred rats) 10 Lophuromys sikapusi (brush-furred rat) plate 2 Louisiana State University 185 Lovelock, James 150, 283 Loxodonta (African elephant) 127 Loxodonta africana see elephant, savanna Loxodonta cyclotis see elephant, forest Lualaba River 110, 116, 118 Lybius chaplini (Chaplin’s barbet) 30 Lycaon pictus see African wild dog lyssa viruses 213 Lystrosaurus 59–61, 60 fig 3.2 Lystrosaurus Assemblage Zone (LAZ) 59 M Maasai Mara 15, 187, 189, 222 table 10.1, 223 MacArthur, Robert 80 Macronycteris vittatus plate 1 Macrotarsomys 91 Madagascar (movie) 93 Madagascar 6, 8–11, 13, 32, 68, 72, 80–83, 86, 134–136, 158 bat colonisations 95–98, 279 evolution in the microcosm 88–98 fauna 54 lemurs 93–95 species diversity 93–95 species radiation 90–93, 157 Madoqua kirki see dik-dik Mafia 82–83, 84–85 table 4.1, 87 Mahé 83, 84 table 4.1 Mahlaba, Themb’alilahlwa xix, 196–198, 208, 238 fig 10.8 Makundi, Rhodes 180, 285

295

AFRICAN ARK

Malagasy bats see bats, Malagasy ecosystem 136 endemics 96, 98 mammals 81, 95 Miniopterus 158 rodents 91 tenrecs 32, 92–93 Malawi 30, 113 Lake Malawi 31, 104 Malolotja Nature Reserve 27 fig 1.7d, 233 fig 10.6, 234 mamba 51 black (Dendroaspis polylepis) 39 mammal(s) diversity 3, 11, 25 giant mammals shaping the landscape 125–148 history of Africa’s mammals 56–78 huge mammals of the past 126–130 invasions: colonisation of Africa 72–75 large mammals 147, 223, 225, 234 decline 221–223, 222 table 10.1 distribution 119 herbivorous 160 impact 195 prediction 221 surviving 234 small mammals and diseases 210–216 that control pest rodents 205–209 Mammal Diversity Database 13, 279 Mammal Species of the World: A Taxonomic and Geographic Reference 9 Mammals of Africa (MoA) 9 mammalian evolution 3, 59, 67, 81 interchanges 73–75 table 3.2 mammoths (Mammuthus) 2 Columbian (Mammuthus columbi) 127 Mammut (mastodons) 2 Mammuthus see mammoths Mammuthus columbi (Columbian mammoths) 127

296

manatee(s) 69 West African (Trichechus senegalensis) 32 Mantenga Nature Reserve 233 fig 10.6, 234 Manyara (lake) 187 Manzini 237 Mara River 139 Marburg’s virus 212 Margules, Lynn 150 marijuana/dagga cultivation 234 marine ecosystems 33 fig 1.8b, 34–36 habitats 67 sediments 193 Markotter, Wanda 210, 211 fig 9.9, 213, 286 marulas (Sclerocaryea birrea) 144 Mascarene archipelago 81 Mascarene Islands 6, 83, 88, 113, 135 Mascarenes 84 table 4.1 mastodons (Mammut) 2 Mastomys see mice, multimammate Mauritania 28, 112 Mauritius 82–83, 84 table 4.1, 88, 134 Mayotte 81, 84 table 4.1, 86 Mbabane 233 fig 10.6, 237 Mbuluzi 147 Mbuluzi Game Reserve 143, 185, 236 Mbuluzi River 236 McCleery, Bob 16, 142–144, 146 fig 6.9, 213 McKechnie, Andrew 63–64 megafauna 128–129 fig 6.1, 130 fig 6.2 and ecosystems 134–136 changing structure and composition of vegetation 137–138 critical ecosystem roles 136–141 cycling nutrients within an ecosystem 138–140 extinct 126–130 impact of humans 130–134 number of species 130 fig 6.2 Megaptera novaeangliae (humpback whale) 33 fig 1.8b Megatherium see sloths, giant

Index

MERS (Coronaviridae) 210, 212 Micaelamys (rock mice) 173 Micaelamys namaquensis (Namaqua rock mouse) 167 mice (Nesomyidae family) 2, 92 climbing (Dendromus) 90, 173 fat (Steatomys) 173 grass (genus Arvicanthus) 49 multimammate (genus Mastomys) 40, 171–173 naked-tailed forest (genus Voalavo) 91 fig 4.4 Namaqua rock (Micaelamys namaquensis) 167 Natal multimammate (Mastomys natalensis) 179 fig 8.4 pouched (Nesomys) (Saccostomus campestris) 72, 91, 174 fig 8.2, 202 pygmy (Mus) 173 rock (Micaelamys) 173 single-striped grass (Lemniscomys rosalia) 203 fig 9.5, 204 soft-furred (Praomys) 119–120 west African (Praomys rostratus) 119 fig 5.8 striped (Rhabdomys pumilio) 49, 51 table 2.1, 167, 173, 177, 203 fig 9.5 Verreaux’s meadow mouse (Myomyscus verreauxii) 34 wood (Hylomyscus simus) 105, 105 fig 5.3 Micropotamogale lamottei (Nimba ottershrew) 92, plate 6 Midgley, Jeremy 34 Mills, Gus 157, 189 Miniopterus aelleni 96 Miniopterus genus see bats, long-fingered Miniopterus grivaudi 96 Miniopterus nimbae plate 1 Miniopterus villiersi (Villiers’ longfingered bat) 158 fig 7.4 Miocene Epoch 58 table 3.1, 73, 74–75 table 3.2

Mitchell, Lorelie 9 Mkhaya Game Reserve 233 fig 10.6, 234 Mlawula Nature Reserve 185, 233 fig 10.6, 234, 236 Mlilwane Wildlife Sanctuary 233 fig 10.6, 234 moas (order Dinornithiformes) 136 Mohéli 81, 84 table 4.1 Moir, Monika 25 mole-rats (Bathyergidae) 173 molecular analyses 89, 95–96, 112, 120 biology 164 biotechnology 18 sequencing 122, 165 techniques 30, 49–50, 54, 69, 91, 122, 164–165, 171 Molossidae see bats, free-tailed Monadjem, Ara xxii Mongolia 112 mongoose 180, 202 table 9.1, 206 dwarf (Helogale parvula) plate 8 marsh (Atilax paludinosus) 32 Meller’s (Rhynchogale melleri) 207 fig 9.8 yellow (Cynictis penicillata) 206 fig 9.7 monkeys 95 platyrrhine 72, 74 table 3.2 vervet (Chlorocebus aethiops) 38 Monotremata/monotremes 60, 63 Mops condylurus see bats, Angolan freetailed Mops leonis plate 1 Mops leucostigma 98 Mops midas see bats, Midas free-tailed Mormopterus (insectivorous free-tailed bat) 88 ‘morphological species’ concept 39–40 Morocco 28–29 Morogoro, Tanzania 179–181 Mortlock, Marinda 211 fig 9.9a moths 155, 159 Eldana 18 Mythimna 18

297

AFRICAN ARK

Mount Cameroon 82 Mount Elgon 122 Mount Kenya 29, 115 Mount Kilimanjaro 29, 123 Mount Nimba 25, 92, 107–108, 108 fig 5.4, 115, 168 mountains 29–30 as barriers 100, 104, 129, 170 as islands 120–124 importance 114–115 movements and barriers 99–106 Mozambique 5, 25, 30, 103–104, 113, 116, 233 Channel 81, 90, 93, 95, 98 Mtsetfwa, Fezile 18, 215 fig 9.11 multituberculata/multituberculates 65–68, 78 Mundy, Peter 20 Muridae family see rats Mus (pygmy mice) 173 Myomyscus verreauxii (Verreaux’s meadow mouse) 34 Myosorex meesteri (shrew) plate 5 Myotis brandtii (Brandt’s bat) 185 Mythimna (moths) 18 myths and misconceptions 217–225 Mzilikazi, Nomakwezi 64 N Naivasha (lake) 104 Naja nigricincta (spitting cobra) 41 Naja nigricincta nigricincta (western barred spitting cobra) 41, 45 Naja nigricincta woodi (black spitting cobra) 41, 41 fig 2.2, 45 Nakuru (lake) 104 Nama karoo 153 Namib Desert, Namibia 27 fig 1.7c, 28 Namib-Naukluft National Park 21, 233 Namibia 35, 41, 45, 113, 198, 200, 225–226 ecotourism 230 fig 10.5 Nature Conservation Amendment Act 229 National Research Foundation of South Africa 64

298

Natron (lake) 104 Natural History Museum, University of Copenhagen 214 Natural History Museum, Utah 223 Nearctic 11–12, 13 table 1.1 Neotropics (South and Central America and the Caribbean) 11–12, 13 table 1.1 New Guinea 80 New World 19, 92 New Zealand 11, 132, 136, 166 Newmark, William 223 Nezara see stinkbug niche(s) 151–152 partitioning 159–166 Niger 28, 116 Nigeria 29–30, 82, 107, 111, 118 Nigerian chimpanzee 118 Nile 28, 116 Nimba (mountain) 25, 92, 107–108, 108 fig 5.4, 115, 168 Nipah virus 213 Noer, Christina 17–18, 17 fig 1.4 North America 2–3, 11, 69, 72, 109, 127, 130, 133 notoungulates 126 Nycteris arge plate 1 Nycteris thebaica see bats, common slit-faced O Oceania 11–12, 13 table 1.1 Ogada, Darcy 22 Okavango 226 Okavango Delta 5, 139 channels 139 fig 6.6, 140 reserves and concessions 227 Old World 19, 47, 92 Oligocene 58 table 3.1, 74 table 3.2 Oribi (Ourebia ourebi) 76–77, 76 fig 3.6 Ornithorhynchus anatinus (platypus) 85 Orycteropus afer see aardvark oryx 112, 123 east African (Oryx beisa) 113

Index

scimitar-horned (Oryx dammah) 28–29 Oryx beisa (east African oryx) 113 Oryx dammah (scimitar-horned oryx) 28–29 Oryx gazella (gemsbok) 113 Oryzorictinae 92 Otocyon megalotis (bat-eared fox) 113 Otomys angoniensis (Angoni vlei rat) 30 Otomys auratus (Southern African vlei rat) 10 fig 1.2, 176 Otomys barbouri 123 Otomys irroratus 8 Otomys jacksoni 123 Otomys karoensis 8 Otomys saundersiae 8 Otomys saundersiae karoensis 8 Otomys tropicalis 123 Otomys typus 123 otter-shrew 32, 93 giant (Potamogale velox) 92 Nimba (Micropotamogale lamottei) plate 6 Oubangui river 103 fig 5.2, 110–111, 111 fig 5.5, 116, 117 fig 5.7, 118 Ourebia ourebi see Oribi Owen-Smith, Garth 286 Owen-Smith, Norman (R.N.) 126, 157, 187, 189, 282, 284 P Palaeocene 58 table 3.1, 74 table 3.2, 95, 193 Palaeoloxodon 127 Palearctic 11–12, 13 table 1.1 Pan paniscus see chimpanzee, bonobo/ pygmy Pan troglodytes see chimpanzee, common Panama Isthmus 77 Pangaea 68, 125 Panthera (big cats) 12, 50 Panthera leo see lion Panthera pardus see leopard Papio anubis (olive baboon) 42

Papio hamadryas (hamadryas baboon) 42 Paraceratotherium (extinct giant rhinoceros) 127 Paramyxoviridae (Henipavirus) 213 Paraxerus cepapi (bush squirrel) plate 4 Passmore, Neville 32 Patterson, Bruce 281 Pemba 82–83, 84 table 4.1, 85, 87–88 Pendjari Biosphere Reserve 166 pelycosaurs 58, 61 periods (geological) 58, 58 table 3.1, 71, 193 Permian mass extinction 58 Permian Period 61 Peterhans, Julian Kerbis 281 Peterson, R.L. 9 Phacochoerus africanus see warthog phylogenetic species concept 40, 280 pigs 28, 69, 74–75 table 3.2, 75, 213 Piper, Steven 20 Pipistrellus hesperidus 96 platypus (Ornithorhynchus anatinus) 85 platyrrhine monkeys 72, 74 table 3.2 Pliocene 58 table 3.1, 74–75 table 3.2 Polemaetus bellicosus (martial eagle) 39 Polyboroides typus (African harrierhawk) 20 population dynamics 170–171, 176–184, 186–187, 191 population regulation 187–191 porcupines (Hystricidae) 173 Potamochoerus larvatus (bushpig) 102 Potamochoerus porcus (red river hog) 102 Potamogale velox (giant otter-shrew) 92 Potamogalidae 93 Praomys (soft-furred mice) 119–120 Praomys rostratus (west African softfurred mouse) 119 fig 5.8 Prince Edward island 82 Principe 82, 84–85 table 4.1, 86 Procavia 70 Procaviidae family see hyraxes Protea nana 34

299

AFRICAN ARK

Protoxerus stangeri (forest giant squirrel) 101 Pseudoryx nghetinhensis (saola) 52 Pteropus species see flying foxes Pteropus subniger (lesser Mascarene flying fox) 88 Python natalensis (rock python) 39 R r/K-selection 171–172, 176, 186 rabies 22, 210, 213 radiation 90–93, 98–99, 157 adaptive 61, 65, 71, 89, 95 local 78, 99 small mammal radiation 159 species radiation 90–93, 157 rainforest(s) 24, 28, 92, 104, 111, 114, 124, 282 bats 168 equatorial 25 lowland rainforests 25 mountainous 90 tropical 22, 25, 32, 102, 107, 111, 190 ratites 136 rats (Muridae family) arboreal tree rat (Thallomys paedulcus) plate 3 black/house/roof/ship (Rattus rattus) 206 brown (Rattus norvegicus) 208 brush-furred (Lophuromys) 10 brush-furred (Lophuromys sikapusi) plate 2 cane (Thryonomyidae) 173 giant jumping (Hypogeomys antimena) 91, 91 fig 4.4 giant (Cricetomys) 90 marsh (Dasymys) 10 veld (Aethomys) 173 vlei see vlei rats Rattus norvegicus see rats, brown Rattus rattus see rats, black red-legged sun squirrel (Heliosciurus rufobrachium) 102 ‘Red Queen Hypothesis’ 156

300

red river hog (Potamochoerus porcus) 102 Red Sea 103 Redunca (reedbuck) 13 reedbuck (Redunca) 13 Reeder, Diane 9 refuge from a changing climate 108–114 forest refuges 109–111 desert refuges 112–114 refugia 108, 110–112, 114–115 Reilly, Liz 234 Reilly, Ted 234, 235 fig 10.7 reproduction and survival 173–176 La Réunion 83, 84 table 4.1, 88, 134 Rhabdomys pumilio see mice, striped Rhabdoviridae 210, 213 rhinoceroses 2, 28, 56, 69, 126, 128 fig 6.1b, 136, 163, 196, 202 table 9.1 black (Diceros bicornis) 151, 162 extinct giant (Paraceratotherium) 127 poaching 234 white (Ceratotherium simum) 151, 162, plate 13 Rhinolophidae family see bats, horseshoe Rhinolophus see bats, Rhinolophus Rhinolophus fumigatus (Rüppell’s horseshoe bat) 48 fig 2.4 Rhinolophus hillorum plate 1 Rhinolophus sakejiensis 54 Rhynchogale melleri (Meller’s mongoose) 207 fig 9.8 Rift Valley see also Great Rift Valley map 103 fig 5.2 rights to wildlife resources 229–232, 238 rivers as barriers 115–120 barriers to small mammal movement 119–120 relationship with great apes 116–119 RNA 46 roan antelope (Hippotragus equinus) 100, 101 fig 5.1, 123–124, 140, 162, 190 fig 8.7, 191 Roaring Forties 82

Index

Roberts, Austin 8, 50, 63 Roberts Birds of Southern Africa 50 rock python (Python natalensis) 39 rodents caviomorph 72 outbreaks 177–183 Rodents of Sub-Saharan Africa 121 Rodrigues (island) 82–83, 84 fig 4.1, 88, 134 Root, Richard 151 Round Island 134 Rousettus aegyptiacus (Egyptian fruit bat) 212 Rukwa (lake) 163 Ruwenzori Mountains 29, 123 Rwanda 29, 104, 110 S sable antelope (Hippotragus niger) 100, 101 fig 5.1, 190 Sahara 28, 30, 98, 112 Sahel 113, 182 Sanaga River 110, 117 fig 5.7, 118 São Tomé 82, 84–85 table 4.1, 86 saola (Pseudoryx nghetinhensis) 52 SARS-CoV-2 (Coronaviridae) 212 Saudi-Arabia 212 Sauromys petrophilus (Roberts’ flatheaded bat) 63 sauropsids 58 Savanna Research Centre 143 savanna(s) 18, 22, 24–32, 26 fig 1.7, 100–114, 120, 123–124, 141–144, 151, 156, 159–160, 178, 180 arid 164–165, 224 ecosystems 16, 187 grassy 173 Guinean 191 moist 31, 102 partitioning 162 subtropical 168 scavengers (scavenging animals) 19, 21, 35, 177 Schoeman, Corrie 152–154, 157–158

Sciuridae see squirrels Sclerocaryea birrea (marulas) 144 Scotophilus nux plate 1 scrub hare (Lepus saxatilis) 14 sea snakes (subfamily Hydrophiinae) 62–63 seals Cape fur (Arctocephalus pusillus) 35 Selous Game Reserve 32 Senegal 29, 104, 110, 174, 182 Senegalia nigrescens see knob-thorns Serengeti ecosystem 19, 180, 187, 284 grasslands 5 Serengeti Biosphere Reserve 187 Serengeti National Park 26 fig 1.7a, 137 fig 6.5, 164, 189, 223 population regulation 187 serval 204, 206 Seuz 6 Seychelles 6, 82–83, 84 table 4.1, 88, 134, 218 Shapiro, Julie 213–215, 214 fig 9.10 Sherman traps 121 fig 5.9, 144, 184 Shewula 236 Shimoni bat lyssavirus 213 shrew (genus Crocidura) 5, 25, 42, 55, 160, 162, 167 elephant-shrew 64, 69 insectivorous shrew (Crocidura canariensis) 83 (Myosorex meesteri) plate 5 on Principe (Crocidura poensis) 86 on São Tomé (Crocidura thomensis) 86 Siberia 185 Sibley, Charles 50 Sierra Leone 24, 102, 107 Silhouette Island 218 Silk Road 196 Simpson, George Gaylord 80 sitatunga (Tragelaphus spekii) 32 sloths 135 giant (Megatherium) 2, 126 Xenarthra 126

301

AFRICAN ARK

Soarimalala, Voahangy 9 Socotra 82–83 Sokoine University of Agriculture Pest Management Centre 285 Somalia 28, 113 Somaliland 28 Sorris Sorris Conservancy 230 fig 10.5 Soulé, Michael 222–223 South Africa bat communities/niches 154 small mammal communities 166 South African Frogs 32 South America 2–3, 11, 14, 17, 68–69, 72, 126, 130, 132–133, 135, 229 southern tree hyrax (Dendrohyrax arboreus) 102 Soutpansberg 168 speciation xxi–xxii, 41–42, 48, 78, 105, 107, 114–115, 124, 245 biogeographic processes 280 by geographic isolation 42–43, 55 climate and plate tectonics 282 in situ 88 instability 44 Rhinolophus bats 49 species concepts 39–40, 45, 280 species diversity 93–95 species names, changing 53–55 spitting cobra (Naja nigricincta) 41 black (Naja nigricincta woodi) 41, 41 fig 2.2, 45 western barred (Naja nigricincta nigricincta) 41, 45 springbuck (Antidorcas marsupialis) 224 fig 10.3 squirrels (Sciuridae) 173 bush (Paraxerus cepapi) plate 4 flying (anomalurids) 5, 72 forest giant (Protoxerus stangeri) 101 Gambian sun (Heliosciurus gambianus) 104 mutable sun (Heliosciurus mutabilis) 102 red-legged sun (Heliosciurus rufobrachium) 102

302

St Lucia 42 Stable isotope analysis 165–168, 284 Steatomys (fat mice) 173 Stenseth, Nils 196 Stephanoaetus coronatus (crowned eagle) 39 stinkbug (Nezara) 204, 205 fig 9.6 Stoffberg, Samantha 48 Stone Age paintings 133 StopRats 199, 205, 207 sub-Antarctic Indian Ocean 82 super-organisms 149–150, 191, 283 Swanepoel, Lourens 206–207 Swati society 237 Swaziland see Eswatini Symes, Craig 166–167 synapsids 58, 60 Syncerus caffer see buffalo, African/ Cape Systemae Naturae 51 systematics 34, 49–50, 54, 126, 280, 282 T Tachyglossidae see echidna Tadarida aegyptiaca see bats, Egyptian free-tailed Tanganyika (lake) 104 Tanzania 5, 29, 83, 102, 104–105, 113, 163, 179, 187, 198, 200, 222 fig 10.1, 223 Taphozous mauritianus (Egyptian tomb bat) 88, plate 1 Tarangire National Park 187 Tauraco corythaix (Knysna turaco) 41 Tauraco livingstonii (Livingstone’s turaco) 41 Taurotragus derbianus (giant eland) 70 Taurotragus oryx (eland) 190 taxonomy 51, 53, 55, 164, 281–282 Taylor, Peter 8–9, 19, 121–123, 121 fig 5.9, 168, 204, 281–282, 285 Tenrec ecaudatus (common tenrec) 92 tenrecs 9, 69, 89–90, 92–93 common (Tenrec ecaudatus) 92

Index

large-eared (Geogale auritus) 92 Madagascar/Malagasy 32, 92–93 Tethys Sea 70, 72–73 Thallomys paedulcus (arboreal tree rat) plate 3 therapsids 57–59, 61–62, 67, 78, 281 thermo-regulation 35 Thomson’s gazelle (Eudorcas thomsonii) 164 Thryonomyidae (cane-rats) 173 Tibesti mountain 30 Togo 107 topi (Damaliscus lunatus jimela) 163, 164 fig 7.6 tortoises 25, 58–59 Aldabra (Aldabrachelys gigantea) 134, 135 fig 6.4 giant Aldabrachelys 135 Cylindraspis 134 Toussaint, Dawn 63 Tragelaphus oryx (eland) 140 Tragelaphus spekii (sitatunga) 32 transfrontier conservation 223, 226, 286 trapping 180 trapping rodents 196 community trapping 200 traps camera traps 146 fig 6.9 insect traps 154 kill-traps 200 live-traps 173, 184 see also Sherman traps Triassic Period 61 Trichechus senegalensis (West African manatee) 32 Tristan da Cunha 82 Tropical Biology Association 96, 136 Tsavo National Park 15, 222 table 10.1 tsessebe (Damaliscus lunatus) 140, 162, 190 Tunisia 28–29, 112 turaco Knysna (Tauraco corythaix) 41

Livingstone’s (Tauraco livingstonii) 41 Turkana (Lake) 104 Turner, Andrew 34, 52 U Uganda 29, 37, 44, 102, 104, 118, 122, 124, 221, 222 table 10.1 Unguja 82–83, 84 table 4.1, 87 ungulates 28, 70, 157–164, 166, 189 even-toed ungulates (order Cetartiodactyla) 69, 127 hoofed 126 migratory herds 194 odd-toed ungulates (order Perissodactyla) 126–127 University of Antwerp 119 University of Cape Town 142, 153 University of Copenhagen 18 Natural History Museum 214 University of Eswatini 143, 196 University of Florida 142, 213 University of Greenwich 197 University of KwaZulu-Natal 152 University of Pretoria 63, 284 University of Swaziland see University of Eswatini University of the Free State 121, 281 University of the Witwatersrand 34, 126, 151, 166, 218, 284 Department of Zoology 218 fig 10.1 University of Venda 206 UNIVISA 225 Unwin, Mike xix, 286 upland habitats 29–30 Upper Guinea (rain)forest 31, 105, 107, 111, 118 US Centers for Disease Control and Prevention 212 V Venda 204, 207 Vhembe Biosphere Reserve 19 Victoria (lake) 44, 104 Vietnam 52, 197

303

AFRICAN ARK

Virunga National Park 106 vlei rats (Otomys) 10, 120–121, 173, 176, 282 Angoni (Otomys angoniensis) 30 Otomys barbouri 123 Otomys irroratus 8 Otomys jacksoni 123 Otomys karoensis 8 Otomys saundersiae 8 Otomys saundersiae karoensis 8 Otomys tropicalis 123 Otomys typus 123 Southern African (Otomys auratus) 10 fig 1.2, 176 Voalavo (naked-tailed forest mouse) 91 fig 4.4 Von Humboldt, Alexander 149 vultures 19–22 African white-backed (Gyps africanus) 19–20, 20 fig 1.5 Cape (Gyps coprotheres) 21 Gyps 20 turkey (Cathartes aura) 20 The Vultures of Africa 20 W warthog, African (Phacochoerus africanus) 14, 160 waterbirds 31 Watson, James 46 Western Cape, South Africa 8, 77 western tree hyrax (Dendrohyrax dorsalis) 102

304

whale 35 humpback (Megaptera novaeangliae) 33 fig 1.8b Whittaker, Robert 151 wildebeest see blue wildebeest Wildlife dispersal corridors 227 Wilson, Don 9 Wilson, Edward 80 Wilson, Gregory 88 wing shape (bats) 153–154, 153 fig 7.1, 154 World Health Organisation 210 Wu, Yonghua 157 X Xenarthra 126 Y Yersinia pestis (Black Death) 195 Yucatán Peninsula, Mexico 56 Z Zaire see Democratic Republic of the Congo Zambezi 116, 225 River Basin 226 Zambia 30, 54, 113, 116, 225–226 Zanzibar 83, 84 table 4.1 islands 87 zebra (Equus burchelli) 28, 69, 162–164, 190–191, 226, 230 fig 10.5b, plates 11&12 Zimbabwe 30, 113, 225–226, 231 zoonotic diseases 210, 212–213