Chapter 1

Africa Background to Exuberance

1.1

Outline of Zoogeography

A delineation of the zoogeography of Africa was attempted rst by Schmarda in 1853. Excluding the northern littoral he divided the continent into three broad regions: Sahara, West Africa, and High Africa. But it was Wallaces division in 1876 which Chapin (1932) described as surprisingly accurate (Fig. 1.1). Wallace had described a West African subregion as stretching eastward as far as the sources of the Upper Nile and the mountains forming the western boundary of the basin of the great lakes. . . Its southern limits are undetermined, but are probably somewhere about the parallel of 11 S Latitude. He showed how the western subregion is largely encircled by the eastern, the latter extending across the Sudan to the Niger Bend and Senegal River, separating the subregion from the desert. The Ethiopian Region, comprising Africa south of the Sahara and part of Arabia, has stood with few modications. Chapin divided it into two subregions: the West African Subregion, which includes a broad belt along the Gulf of Guinea, almost the entire Congo Basin (except the High Katanga), and most of Uganda. The remainder formed the East and South African Subregion. The great rain forest, termed the Guinea Forest Province, is divided into two districts: the coastal forest around Cape Palmas to the west, referred to as the Upper Guinea Forest District; and the Lower Guinea Forest District, including the forested area of the Congo Basin with the lowland forests of Uganda as outliers, the western parts of Uganda not being essentially East African (Fig. 1.2). During the mid-Tertiary Africa had reached its present latitudinal position from further south when the equator passed through the present-day Sahara and the ancient peneplane surface of the central African plateau exed and warped, the east African hinterland swelled upwards and the Congo sank into a basin altering drainage patterns. Further uplifting at the end of the Miocene raised the central plateau to its present level and the generally high altitude of equatorial East Africa formed a water tower feeding the Nile, Zare River, and several basins which have either no outlets to the sea or have outlets into the Indian Ocean. Rifting, which may
C.A. Spinage, African Ecology - Benchmarks and Historical Perspectives, Springer Geography, DOI 10.1007/978-3-642-22872-8_1, # Springer-Verlag Berlin Heidelberg 2012 1

Africa Background to Exuberance

Fig. 1.1 Wallaces Ethiopian Region. 1, East African; 2, West African; 3, South African; 4, Malagasy (From Wallace 1876)

be seen as the primary cause of East Africas diverse ungulate fauna by causing isolation of populations, began 1512 Mya (million years ago) in southern Kenya, compared with 3020 Mya in the northern sector of the Rift, earlier than in Tanzania where rifting began in the Pliocene some 7 Mya. Major rejuvenations occurred in southern Kenya 52.5 and 0.60 Mya contemporaneous with Tanzanian rifting, and 21.5 Mya in northern Kenya. This last Pleistocene phase created much of present day rift topography, resulting in the Magadi-Natron and Manyara basins (Grifths 1993). The rise of the eastwest continental divide limited the western Guineo-Congolian climatic and biotic inuence, separating it from the eastern forests by a northsouth band of seasonally dry country experiencing <10 mm rainfall/month for three consecutive months, termed the arid corridor which connects the northeastern and south-western arid areas and reaches east to the Indian Ocean in northern Mozambique. This forms a barrier to the eastwest dispersal of moist forest organisms (Fig. 1.3). Possible faunal migration routes during wetter periods 96.4 and 4.62.4 Mya, would have been northwards over the Kenya Highlands and down the rivers draining eastwards (during the latter wet period Lake Turkana in northern Kenya possessed a much richer riverine forest with western Guineo-Congolian elements), or southwards via the Lake Tanganyika rift along the mountains and valleys of the southern Rukwa rift into the Lake Malawi climatic system, and across

1.1 Outline of Zoogeography

Fig. 1.2 Chapins (1932) subregions of the Ethiopian Realm based on bird distributions but which proved rather satisfactory for mammals and some other terrestrial animals. East and South Africa were classied as one but a separation is shown here, a number of South African mammals being distinct. Chapin divided the subregions further into districts. Filled areas are montane districts

the forest gap in the southern Uzungwa Mountains (Lovett 1993). The potential rate of spread of even the smallest of indigenous animals means that in the million years since the Pleistocene they have had ample time to extend over the whole continent, and thus the present pattern of distribution is essentially one of dynamic equilibrium in which continuous attempts to disperse more widely are prevented by inability to obtain a foothold outside established areas of distribution, whether this be due to climate, topography, lack of suitable resources, or competition (Balinksy 1962). Ecosystems are in a continual state of turmoil in space and time and constant change in the relative favouring of different species in the system enables all of them to persist for a long time. Introducing diary accounts of mid-nineteenth century travellers in Liberia, Fairhead et al. (2003) claimed the documents would astonish even the knowledgeable in many ways, referring to the travellers Seymour and Anderson describing an

Africa Background to Exuberance

Fig. 1.3 The arid corridor. Cross-hatching shows area where rainfall is <10 mm per month in at least three consecutive months (After Balinksy 1962)

area as open savannah populous, prosperous, cultivated, and vibrant with trade, now a celebrated tropical forest reserve iconic of present impressions of it as a natural forest Arcadia. In western Africa the habitat reversals have often a much longer history but for those ecologists grounded in eastern, central, and southern Africa, this comes as no astonishment, for we know that many of the best faunal areas, for the most part now protected or quasi-protected, are those areas evacuated of their human occupants during sleeping sickness control measures at the beginning of the twentieth century. Thomas (1946) in his Uganda studies stressed the importance of the human inuence in African ecology, showing how not only was vegetation affected by past settlement but also the soil down to its colour, many red soils being indicative of former settlement, and noting in respect of virgin forest . . . there does not seem to be much virginity left in most parts of equatorial Africa, for little of the vegetation is in the climax stage. But despite changes wrought by man Africa remains a continent outstanding for its exuberance of life, both in numbers and variety of ora and fauna.

1.2 Species Richness

1.2

Species Richness

A pattern of abundance which has existed for more than 270 million years and broadly applying to all forms of life, species richness is immense in the wet tropics, diversity declining rapidly with increasing latitude. During cold periods in the earths history diversity has been compressed towards the equator, to expand again during warm intervals. Numbers of theories have been proposed to explain this pattern and Humboldt suggested in 1808 that energy was the cause of global species richness patterns, but a plausible mechanism that might link energy to species richness was wanting (Gillman and Wright 2007). However, by reference to plants molecular evolution has been demonstrated to be more than twice as fast in the wet tropics, apparently driven by productivity. Higher production allows more opportunities for mutation and formation of new species, but other factors modify the underlying driving force. Most diversity of mammalian herbivores is shown by the Family Bovidae with 91 species of large herbivore in sub-Saharan Africa, although only 38 occur in West Africa, and of which some 80% of the total are antelopes. This profusion of species is occasioned by six differing biotic types, or vegetational forms, occurring in Africa broadly in successive bands either side of the equator to provide a variety of habitats in which evolution can take place (Fig. 1.4). No other continent straddles the equator in this manner to give such variety of biotic types and the distribution of different species of bovid, particularly antelopes, is related to them rather than to plant species classications, although the two are complementary. The parallelism of these zones breaks up in the north-east and south-east of the continent where more arid conditions intervene at opposite ends of the arid corridor, creating increased diversity by mixing species (Table 1.1 and Fig. 1.5). If antelopes stemmed from a forest origin, then relating species to the different broad vegetational zones is fundamental to understanding their diversity. It is not a random evolution of different types radiating outwards from a forest environment but relates to the physiological and nutritional conditions posed by each zone, although these may no longer be in evidence for some species. To these biotic zones we could add gallery forest, which tends to harbour specic assemblages within a major biotic type. In the past two centuries the grasslands of Africa within both dry and moist savannah1 woodland carried the highest herbivore biomass of any natural community, and whereas the pachyderms may have dominated in terms of weight within certain areas, the greatest absolute numbers and diversity of species was provided by ruminant ungulates, of which three remnant communities remain: in the southern Sudan, western Tanzania, and Botswana. Preliminary studies in 1954 in Kenyas Nairobi NP gave an estimate of mixed herbivores on Themeda-Acacia wooded grassland of 3135 animals/km2, equal to a biomass of 11,34013,608 kg. Similar levels of biomass occurred also in the Lake Edward area of Uganda and DR Congo, exceeding this by more than ten times in areas where hippopotamus concentrated (vide infra). American bison Bison bison are calculated to have roamed the prairies at 7.710.8/km2, the estimated carrying capacity being 7.78.1 cattle/km2, with the most productive area reaching 10.8 (Petrides 1956).

Africa Background to Exuberance

Fig. 1.4 The main broad vegetation regions

Total biomass density is positively related to rainfall. Similar relationships apply generally also to the population biomass densities of individual ungulate species, thus the inference is that herbivore biomass is governed by net annual aboveground primary production (the food supply) in turn governed by rainfall. A unimodal rainfall regime in West Africa and a bimodal regime in East Africa may account for large game species being less abundant in the former area, the regime affecting the growth of grass cover necessary to sustain large populations of wild herbivores ` (Le Houerou 1989). A lesser diversity of species in West Africa, on the other hand, is due to its uniform topography and latitudinal zonal vegetation (Spinage 1986). An explanation for the great number of species of birds and mammals in the tropics has been suggested to be the many shapes and sizes of plants of the tropical forest, but more recent arguments for the prevalent speciation in tropical forest animals favours a mechanism of parapatric speciation, the evolution of reproductive isolating mechanisms occasioned by a population entering a new niche or

1.3 The Abiotic Substrate and Its Vegetation Table 1.1 The biotic types of Africa Biotic type Phytogeographic class

Approximate area (km2) 4,213,000

Lowland rain forest

Moist savanna woodland

Dry savanna woodland

Sub-desert and desert Mediterranean Montane forest

715,000 5 (includes Afro-alpine) a Some species occur in more than one biotic type, the gures give the total for the type

Guineo-Congo region (Congo domain, Usambaro-Zululand domain) Sudano-Zambesian region (Sudanian and Zambesian domains) Sudano-Zambesian region (Sahelian and Afro-oriental domains and South-West Arid) Saharo-Sindian and Karoo-Namib regions Mediterranean region (Mauritanian domain) Cape region All regions and all domains except Usambaro-Zululand domain

Number of antelope speciesa 15

9,889,000

32

4,335,000

30

8,048,000 71,000 (Cape)

13 8

habitat within the range of the parent species. In mature forest the fauna is rich and strongly stratied resulting from the microclimate, demonstrated by the occupation of different levels by mammals, birds, reptiles, amphibians, and insects (Fig. 1.6); and the lowland forest mammalian and bird faunas are more or less distinct from those of both savannah and montane (Moss 1969).

1.3

The Abiotic Substrate and Its Vegetation

Terrestrial tropical ecology is dominated by the diel rhythm (24 h changes) as opposed to annual seasonal changes, and at the equator the amount of incident solar energy is a more or less constant environmental feature. The most important ecosystem processes involve the abiotic part of the system minerals and water recycling. Changes in the nature and amount of predation, competition, herbivory, migration, emigration, and immigration, are all important and will lead to changes in community composition, but changes in the hydrological cycle or in the interactive processes of the mineral cycle potentially have more profound effects on the structure of the system (Walker 1989). Worthington (1938) pointed out it was an error to suppose the tropical conditions of Africa implied the existence of an exuberant vegetation and rich soil. With some exceptions of limited area, soil south of the Sudan is generally poor, and in the arid and semi-arid regions which make up perhaps half of the total area of the continent, has little humus, while calcium and phosphorous are decient over wide areas. In the moist evergreen forest of West

Africa Background to Exuberance

Fig. 1.5 The colonization of habitat types (Corrected from Spinage 1986)

Africa the amounts of all exchangeable nutrients in the top 30 cm of soil, excepting phosphorous, are considerably less than the amounts stored in mature forest fallows, that is, forest cleared for cultivation and after cropping left to fallow. Soils under moist evergreen forest are poor and richer under moist semi-deciduous forest, but due to heightened metabolic activity moist tropical forest can produce 12.35 t/ha of dry matter compared with slightly less than 2.47 t/ha for temperate hardwoods.

1.3 The Abiotic Substrate and Its Vegetation

Metres 45 Metres 45
EMERGENTS

40

40

35

35

30

RED COLOBUS MONKEY

GIANT FOREST SQUIRREL

30
MAIN CANOPY

PELS FLYING SQUIRREL

25

TREE HYRAX
GREEN MAMTBA

25

20
BOSMANS POTTO

PUTTY-NOSED MONKEY BLACK COLOBUS MONKEY LESSER BUSH BABY

MONA MONKEY GENET TWO-SPOTTED PALM-CIVET

SUN SQUIRRELS

GAMBIAN AND RED-LEGGED

20
UNDERSTOREY

15
AFRICAN PYTHON TWIG SNAKE

TREE SNAKERS

15

GREEN-BELLIED FANGOLIN GREEN THEE VIPER

AFRICAN PYTHON

10

BOOMSLANG

SIDE-STRIPED SQUIRREL
AFRICAN PYTHON

10

5
GREEN SNAKER BEAUTY SNAKE

5
MAXWEELS DUIKER AFRICAN CIVET POUCHED OR GAINT RAT RED RIVER HOG BROWN MONGOOSE CUTTING GRASS BRUSH-TAILED PORCUPINE
PUFF ADDER BURROWING VIPERS

GINT GROUND PANGOLIN

SHRUB LAYER
BALCK BACKED DUIKER BLACK DUIKER

FILE SNAKE

CALABAR GROUND PYTHON

FOREST CLEARINGS

FOREST EDGE

RHINOCEROS VIPER

BLACK COBRA

HIGH FOREST

GABOON VIPER

Fig. 1.6 Forest stratication of some mammals and snakes (From Moss 1969)

The Sahel is a latitudinal zone with 300650 mm annual rainfall, lying between Subdesert to the north with 100300 mm and the narrow Sudanian zone to the south with 650900 mm. South of this is the woodland zone with 9001,200 mm. The majority of the area is dominated by annual species of herbs and grasses due to the extreme climate in which a short rainy season is combined with a high evaporationrainfall ratio. The generally poor soil implies that only in the northern Sahel is production limited by water availability while elsewhere nutrient availability is the limiting factor. Normally rates of nitrogen xation and nitrication are low because of the dryness of the soil, mineral nitrogen being released most rapidly when soil is wet. Thus rainfall has an overriding inuence, vegetative growth almost ceasing during dry seasons due to lack of water. But in the Rukwa Valley grasslands of Tanzania, Backlund (1956) found that grasses such as Cynodon dactylon (L.) Pers. could remain green in the dry season when the surface soil was baked dry because the roots penetrated more than 50 cm to a depth which held moisture throughout the dry season. Almost half of Africa consists of grassland, although most is anthropogenic in origin (Skarpe 1986) but often nitrogen supply limits growth. The complex dynamics of litter decomposition in the tropics is not well known. Leaf litter provides a substrate for the release of inorganic nutrients and mulches the soil surface, inhibiting leaching of these nutrients from the surface. Removal of grazing and browsing animals enhances this process. Signicant biogenic production of ozone may occur at the end of the dry seasons when rains wet formerly dry soils and trigger microbial production of nitric oxide, but the type of rainfall characterized by very few dry months and a few very wet, frequent in Kenya and Uganda, is found

10

Africa Background to Exuberance

only exceptionally in west and central Africa. Heavy rain in a short period falling on soil made friable by long exposure to the sun can leach out some of its most valuable constituents and thus become a potent cause of soil deterioration. Due to the preceding long dry season and consequent accumulation of organic matter in the soil, in the dry regions of East Africa a second rains, although lighter, appears ecologically more important than the previous heavier rains, thus observed differences in rainfall are not necessarily correlated with differences in biological phenomena. Experiencing two dry seasons, one of 56 months, the other two or three, the second rains are more predictable in occurrence and of providing a given amount, thus the activity of plant and animal species is stimulated to maximum growth and reproduction at this time. A notable example is provided by the larger dung beetles, Heliocopris sp., Catharsius sp., Scarabaeus sp., and Onitis sp., which are more numerous in the second rains (Tyrell and Coe 1974). The distinctive feature which springs to mind when considering the ecology of tropical Africa is the lack of an annual cold period equivalent to the temperate zone winter, but this is replaced by a dry interval with signicant seasonal changes. Studies of annual biomass uctuation in the Ivory Coast Guinean savannah show that while most major consumer groups of arthropods, amphibians, lizards, snakes, birds, insectivores, and rodents, are present throughout the year, their populations are generally reduced during the short dry season, reaching lowest levels following ` annual bush res and increasing again with the rains (Bourliere and Hadley 1970). African oras tell one almost nothing of plant phenology, when owering and fruiting takes place, leaf fall, and regrowth. Flowering in some trees precedes the rst rains, in others it follows the beginning of the rainy season. Caducifoliate trees in the savannah shed their leaves annually like temperate species, generally producing new leaves and owering before the end of the dry season after about 100 days dryness without waiting for the rst rains. The same is true of many forest trees. Koechlin (1961) considered the causative stimulus of this regrowth was undetermined, depending as it does on the water reserves of the plant or those existing in the soil, but it is now attributed to an endogenous genetic response (Dunlap et al. 2004). The probability is that growth is simply continuous, an inherent cycle which is going to take place whatever the conditions, although it can be induced by re leading to the suggestion that it may be a rise in temperature which provides the stimulus for regrowth. Moss (1969) notes the most striking and obvious difference between closed forest and savannah is the formers sheer bulk of vegetation, with dry weights recorded for above ground vegetation of up to ve times compared to savannah, and of which 75% is woody material. The difference is associated with a contrast in structure. Except in the denser savannah woodland there is no closed canopy and the shrub layer is not continuous. The grass-herb or ground layer varies considerably in oristic composition, height and continuity, and there is an almost complete absence of tree climbers. These differences in the savannah imply important differences in nutrient and water properties, enhanced by the seasonal aspect of many of the savannah plants. In contrast to forest, savannah soil levels can dry out rapidly after rains cease, which drying may be augmented by the seasonal character

1.3 The Abiotic Substrate and Its Vegetation

11

of many savannah plants. This has important effects on nutrient cycles, which are seasonal compared with the relative continuity of those under forest, and water deciency at the beginning and end of rains may have a markedly inhibiting effect on nutrient uptake by the vegetation, possibly inuenced also by type of soil. Although grass and herbs are such an important part of the savannah vegetation trees play the most signicant role for they store the bulk of the water and some ve times the nutrients, containing a much higher proportion of calcium than grasses and herbs, limitations of which can seriously affect the phosphate balance of the soil. The average mature equatorial forest of the Congo and Ghana contains about 30% greater weight of vegetation than the average even-aged 100-year-old temperate hardwood forest. Largely because the wood is richer it contains very much more potassium, sodium, and calcium (Rennie 1955). Plant diversity in Africa is higher and its phenology controlled by water availability in contrast to temperature, for rainfall variability tends to be high. Nutrients tend to be low rather than high. Overall the vegetation is seen as inherently structurally unstable with a wide range of possible tree cover and rapid changes, compared to the vegetation being seen as tending to a stable climax of forest or grassland (Scholes et al. 2003). Thus productivity in savannahs is thought to be inuenced more by densityindependent factors such as climatic variation and episodic events such as drought. In general primary production and animal density in the savannahs are correlated with mean annual rainfall, but the relationship is complicated by soil type as inuenced by base geology and soil factors may suppress or exaggerate effects of an erratic climate. Savannahs with nutrient rich, or conversely nutrient decient, soils, support different types of vegetation and densities and varieties of herbivores. An example of the former is the acacia savannah of East Africa, and of the latter the miombo woodlands of east central to southern Africa. Except in very low rainfall areas as in the northern Sahel, poor soils support a vegetation of woodland and grassland of low nutritional value for grazers. Relatively low densities of herbivores are able to exploit this environment and their impact on plant biomass and the relative balance of ligneous and herbaceous species may be only marginal. Savannahs with higher quality soils support a higher density and greater diversity of herbivores because of the higher nutritional value of the food resource, and stocking densities may be sufciently high to suppress the standing crop of herbaceous material and/or suppress woodland encouraging grassland (Bell 1982). Moreau (1966) considered that Quaternary environments, particularly their changes in climate, were the major determinants of the present distribution of organisms in Africa. Compared to some other regions of the humid tropics, African forests are poor in species of plants, birds, and insects, but not mammals. Yet the environment of Africa appears just as suitable for development of forest, suggesting the cause of species poverty must be historical. Widespread extinction of lowland forest species may have occurred when forest extent was greatly reduced, probably during arid interludes, but repeated fragmentation and coalescing does not seem to have increased the number of species possibly because durations of the oscillations

12

Africa Background to Exuberance

were too short. Illustrating the poverty of the West African forest ora, of the 41 taxonomically isolated forest species of African ebony Diospyros, 24 are endemic to the Congo Forest Block, 22 occurring in, and 11 conned to, a coastal strip 260 km wide extending from south-eastern Nigeria to the mouth of the Zare River, the total area of which is less than that of the Guinea Forest Block, which has four endemic species only (White 1962). Grubb (1977) emphasized plant species richness was attributed to the great potential habitat diversity at and immediately above the soil surface, where plants can adapt and specialize through competition with other plants and also with animals. Disturbance whether by windthrow or animal burrowing inuences the diversity of microhabitats for establishment and regeneration, for the inuence of interspecic competition on both species survival and evolutionary changes in gene frequencies within populations is concentrated during phases of reproduction, establishment, and early growth. Ultimately specialization of the regenerative niche in evolution results from accumulation of species richness within the plant community. High niche specicity, if biotically mediated, implies the competitive environment for a species is highly restrictive but continually changing over evolutionary time. Survival of species would be dependent on maintenance of genetic viability within populations, and the existence of populations with low genetic variability suggests lower niche specicity. Niche specicity may be relatively rare among some, at least, of the rare species which comprise the vast majority of mixed rain forest ora, thus it is among these that non-equilibrium phenomena should be expected. Ashton (1989) asks what, other than chance, could cause the extinction of parthenogenetic rainforest species in which the population density is too low to be affected by density controlling factors?

1.4

Animal and Plant Interactions

Compared with South America and its rich Amazonian species diversity, the biota of Africa is relatively depauperate. Africa has an estimated 25,00030,000 species of tropical owering plants compared to 55,00060,000 in Asia and 85,00090,000 in South America. An important ecological difference between most African and Australian vegetation may be absence from the latter of signicant numbers of browsers for the last 10,00030,000 years. This may have resulted in relaxation of many selective pressures on plants, now re-imposed by imported domestic stock. A substantial body of productive palatable plants in Australia seems very susceptible to overgrazing, by comparison African systems may have reached a new equilibrium long ago after losing the equivalent body to the pressure of natural herds or from the more recent domestic herding. Some African vegetation seems also more substantially armoured with thorns and spines, but it is unclear to what this may be attributable (Smith and Pickup 1993).

1.4 Animal and Plant Interactions

13

Plants do not succumb passively to grazing or browsing but produce secondary metabolites to protect them from, or limit attack from, pathogens and herbivores. Some metabolites, such as alkaloids and cyanogens, have a direct toxic action, others such as tannins and lignins may reduce digestibility. But likewise herbivores have evolved detoxication mechanisms, dietary toxins being degraded within the ruminant and non-ruminant gut by microbial activity; or they may use the chemicals as cues to avoid the plant. There is evidence to suggest also that herbivore saliva may stimulate growth in some plants, the plant responding to attack by increased growth rather than by defence (Rhoades 1985). Thus ungulate herbivores are not passive consumers but cause changes in the environment by modifying conditions for other organisms above ground, the indirect effects of which may exceed the direct consequences of ows of energy and materials from plants to consumers, making them important agents of change in ecosystems ranging from grasslands to forests. They modify nutrient cycling, inuence primary production, alter patch dynamics, and affect abiotic disturbance (Hobbs 1996). Animals are the greatest distributors of forest tree fruits in DR Congo, Malaisse (1978) providing frequencies of fruit dissemination for rain forest, semi-deciduous forest, transition forest, mountain forest, swamp forest, and miombo woodland. These averaged 3% waterborne, 22.1% windborne, 22.6% fallen (autochory), and 52.2% animal. Tanzanias Serengeti grasslands have been heavily grazed probably for several one thousand years with 6094% of above ground net primary productivity consumed annually (McNaughton 1985), the grasses evolving a variety of responses to promote rapid regrowth of leaves following defoliation. Because grazing is high litter production is low, nitrogen being returned to the soil in urine and faeces. Also, rapidly growing plants contain high levels of nitrogen relative to carbon which is in a form which tends to be more decomposable than in mature plant tissue, and in roots is allocated to shoots following defoliation. Together these factors make the ratio of carbon to nitrogen in the substrate available for decomposition exceed that in the absence of ungulate grazing, which means the soil fauna is more likely to be limited by availability of carbon than nitrogen and as a result immobilization of nitrogen declines, mineralization accelerates, and more nitrogen becomes available in the soil for uptake by plants. During the dry season Serengeti ungulates migrate to the tall grass plains where grass production is much higher than on the short grass plains. As a result a relatively small proportion is consumed and the standing crop fails to attain the concentrations of nitrogen that it does on the short grass plains, partly due to the relatively nutrient-decient sandy soils of the tall grass plains and partly from dilution of regrowth by a large standing crop of mature grass. This means large quantities of litter with high levels of carbon are added to the soil, and because grazing increases production these quantities exceed those which would be expected in ungrazed grassland. This creates a reverse effect to that in the short grass plains, due to the large additions of carbon to nitrogen carbon is relatively more abundant in the soil and microbial growth becomes limited more by nitrogen than by carbon, intensifying competition for nitrogen between microbes and plants. Increased immobilization of nitrogen by the soil fauna reduces its availability to plants as the system becomes clogged by litter. Thus ungulate grazing can

14

Africa Background to Exuberance

accelerate or retard mineralization (Hobbs 1996). Grazing lawns comprise short plants with higher bulk and higher leaf nitrogen concentration, consequently the amount of nitrogen per unit volume is several times higher than in ungrazed areas. Because nitrogen and other nutrients are concentrated in grazing lawns grazing acts to enhance conditions for future feeding as plants regrow (McNaughton 1976). This causes diversity in the landscape. But impact of the herbivores in the dry season in the long grass region of the Serengeti is greatest at the time when above-ground production is largely dead and the plants dormant, thus there is little effect upon plant viability. On the short grasslands the large herbivores depart before the end of the growing season, so the plants have time to ower and seed (Sinclair 1975). An unmistakable characteristic of the African landscape is the termite mound. Only active mounds have a characteristic vegetation and this differs to that of the surrounds and varies within the Zambezian region. The soil nesting Hodotermitidae family together with Trinervitermes occur in such numbers in some areas they remove the grass over large extents of savannah, decreasing the carrying capacity of pastures, promoting soil erosion and desert encroachment over wide areas of South Africa. Sinclair (1975) looked briey at their role in the Serengeti ecosystem. In the short grass areas 51% of production was estimated to be consumed by detritivores of which termites were the most important. Elsewhere it has been calculated 7 kg dry weight of termites can remove 1,170 kg of primary production/year and their biomass can range between 15 and 150 kg/ha.

1.5

Extinctions

It has been suggested major vegetational changes may have taken place following extinction of the giant herbivores some 10,00050,000 years ago, these herbivores having played a major role in structuring the vegetation, but climate was probably more signicant. Fire seems to have little effect on the biogenic emission of carbon dioxide, methane, and nitrous oxide, rainfall and soil moisture seemingly having a much higher inuence, yet unlike the temperate zone forests and grasslands of the Northern Hemisphere the savannahs of Africa south of the Sahara have re and mammalian herbivory imposed upon them to a degree not encountered elsewhere, mammalian herbivory at a higher level having exerted its effects since Miocene times, while association with hominids exceeds that of the Northern Hemisphere by a time factor of 150. A major extinction of mammals, particularly large mammals, took place in Africa very approximately at the date of transition from Acheulian to later human cultures, while similar events elsewhere in the World suggest man was the responsible agent (Martin 1966). For extinctions on the scale which occurred an inuential factor causing them must have been habitat modication on a signicant scale, such as might be caused by burning. Whereas hunting may have had an effect upon large and vulnerable species this is unlikely to have been to the point of extermination on agile species. Klein (1989) argued climatic change by itself was an insufcient

1.6 Refugia

15

explanation for extinction because the species which became extinct in the terminal Pleistocene/early Holocene c110009000 B.P. had survived earlier periods of broadly comparable change. Fossil material from the Lower and Middle Pleistocene is insufcient to indicate whether comparable extinctions took place in these periods. Given drought conditions both man and beast would have concentrated on the remaining water sources and it would have taken little effort to slaughter the larger fauna through pitfalls, ring-burning, or spearing with or without poison, but the ultimate cause of their demise would have been drought.

1.6

Refugia

Formerly the equatorial lowland forests of the Congo Basin and western Africa were considered to be among the most stable ecosystems on earth, and their great oristic diversity interpreted in terms of persistence or very slow change (Vincens et al. 1999). But these forests are now thought to have been subject to drastic oristic modications in response to global climatic changes. During the Quaternary the lowland forests were affected by long time-scale and large amplitude climatic uctuations, the dry cold period of the Last Glacial Maximum leading to fragmentation and isolation of forest communities in refugia and the presence of montane biotopes in the lowlands, but shorter climatic events affected them during the past 4,000 years. Certain sectors of the rainforest are much richer in endemic species and taxa of ora and fauna than others, the richest area comprising the Biafra forest inside the curve of the Gulf of Guinea from the Cross River in east Nigeria to the Sanaga river in west Cameroun, and further south from the southwest Cameroun evergreen forests to those in west Gabon. Slightly less rich is a sector far to the west of the forest block, the Guinea uplands of Guinea and Liberia stretching to the south-east of Liberia and the extreme west of Ivory Coast. South-west Ghana and adjacent Ivory Coast have a number of endemic species also, and the central part of the Congo Republic-DR Congo basin is relatively rich in endemic taxa. This richness is explained by these sectors being located on former refugia (Fig. 1.7) (Maley 1996). Diamond and Hamilton (1980) disagreed with Moreaus conclusions concerning the effects of Quaternary environments on forest, considering there was no reason to suppose montane forest was more extensive at one time previously than at present with connections and exchange between presently isolated areas, but there was a relatively recent spread of forest from refugia. Before about 12000 B.P. forest was much more limited in tropical Africa. Lowland forest was represented by two refugia in West Africa and others in Cameroun/Gabon, eastern DR Congo, and near the East African coast; while there was well-developed montane forest in Cameroun, eastern DR Congo and eastern Tanzania. The highland areas of Kenya and Ethiopia were largely savannah, probably with localized patches of impoverished forest. The refuge areas may have continued to carry forest throughout the Pleistocene, elsewhere alternating moist and arid periods causing major vegetational shifts. The number of

16

Africa Background to Exuberance

Fig. 1.7 Forest refugia (stippled areas) (After Maley 1996)

bird species in refugia at present is believed to be related more to the status of the refugia in terms of area and habitat diversity during periods of maximum contraction than to present environmental conditions. Since about 12000 B.P. forest has spread from the refugia and species of birds have followed at various rates creating gradients of increasing species poverty away from the former refuge areas. The long term persistence of these gradients may be due partly to competitive exclusion. There is no reason to suppose montane forest was at one time much more extensive with connection and exchange of birds between presently isolated areas, but Gregory concluded in 1896 the altitudinally higher fauna and ora of the East African Mountains showed closer afnities with their respective groups in West Africa than with the plains fauna and ora in their own immediate vicinities. Some have cautioned against the theory of forest refuges, seeing them as presenting a too black-and-white picture of complex events and maps of refugia should be regarded as tentative hypotheses only. But Hamilton et al. (2001) consider that for Uganda the refugium theory of forest hotspots is well supported by fossil pollen evidence. The large central refuge of the Congo Basin was riparian, associated with permanence of the Zare River uctuations and its main tributaries, the refuge due not to the climate of the area but to conditions in the rivers distant headwaters. White (2001) refers to intriguing puzzles of the rain forest which may relate to human activities and population dynamics of the Iron Age. Such enigmas as the monodominant Gilbertiodendron dewevrei (De Wild.) J. Leonard forests of DR Congos Ituri and elsewhere in central Africa, the lack of regeneration of certain common species of emergent tree in Cameroun, and the interdigitation of semievergreen, single-dominant moist evergreen and drier-peripheral semi-evergreen forests, the latter with many faster growing species that colonize secondary vegetation. While some persistent refuges clearly existed, and still exist, Grubb (2001) suggested a comprehensive refuge theory for mammals may be neither necessary

1.6 Refugia

17

` nor sufcient to account for many present-day patterns of diversity. Barriere et al. (2005) from a study of the distribution of shrews in CAR, concluded Pleistocene refugia were probably not homogeneous forest blocks but provided by a network of gallery forests. Although gallery forests in north CAR harbour several plant, bird, primate, and large mammal species typical of rainforest 400 km to the south, no typical rainforest shrews of the Zare River Basin nor typical rainforest murid species were detected. This lends credence to the view that Pleistocene refuges would have been composed of a network of forest patches within a forest-savannah mosaic. This northern CAR region is at the watershed zone of the Zare River Basin drainage to the south and the Chari Basin to the north, larger and more mobile species could cross the short intervening distance between the headwaters of often less than 10 km, but not smaller mammals. Similarities between plants and animals of the south-western and northern arid regions provide evidence for a more arid climate in the intervening area in the past. Although there has been a relatively recent connection, this was insufciently long, or the climate was unsuitable, to allow a complete exchange of species. This is shown by the large number of endemic species in the South-West Arid Zone, and to a lesser extent the Somali Arid Zone, and that many of the disjunct species belong to sub-desert rather than true desert forms. The plants and animals of the northern and southern savannahs have both similarities and dissimilarities, the faunal divide known as the Sclater line running from the fringes of the Zare Basin to the Tana River, the great climatic and topographic diversity of the southern savannahs perhaps accounting for the high number of species, but the geographical discontinuity between the dry forests of the two tropics does not exist today as man has intensively deforested the high plateaux of East Africa. The East Coast forests seem to have been isolated from those further west for a long time, but at some stage connections did occur. In the west, forest mammals spread out fairly recently from a small number of refuges in the Guinea Forest Block, and from two large refuges either side of the Congo Basin, the southern Cameroun-Gabon area and Rwenzori-Kivu. Despite minor recent connection, the Guinea Forest Block has always been rather isolated from the Congo Forest Block, but the degree of isolation was less than that of the East Coast forests. Many East Coast forms of lowland forest plants, birds, and butteries, are distinctive, and in the west there tend to be centres of endemism and species richness in the same localities as for mammals. Hamilton (1976) considered a former forest connection across DR Congo probably pre-dated 25000 B.P., and could be as early as 75000 B.P., representing the minima for isolation of disjunct vertebrate and invertebrate populations and indicating a wetter regime. The isolation of the Congo Forest Block from that of the Guinea and East Coast forests probably dates back to at least hundreds of thousands of years in the former and millions for the latter. There is some pollen evidence to suggest a drier climate in the Omo basin of Ethiopia at about 2 Mya. Some minor movement of species between the Guinea and Congo Forest Blocks has probably taken place since 12000 B.P.

18

Africa Background to Exuberance

1.7

Species Richness Considered

There are three main montane centres of species richness and/or endemism: Cameroun, eastern DR Congo, and Tanzania, especially Tanzanias Usambaras and Ulugurus which appear to have been colonized by long-distance dispersal as opposed to being relics of a continuous forest area. About 20000 B.P. the continent was arid with lowland forest restricted to six small blocks, three very small blocks along the Guinea Coast, one on the west coast, one in eastern DR Congo, and a narrow strip bordering the Indian Ocean. In a wet phase of about 8000 B.P. the two former areas expanded to cover the Guinea Coast and the Congo Basin but not enveloping the eastern montane areas before retracting again in historical times. Denys et al. (1985) demonstrated maximum mammalian species diversity in the Rift Valley in the Pliocene 21.8 Mya, with 23 bovid species and 34 hominids found at Omo. At the beginning of the Pleistocene rifting and climate provoked big changes, reducing diversity to ten bovid taxons and two hominids, returning it to equilibrium after the extraordinary phase of Pliocene diversication which appears to have been induced more by tectonic activity isolating populations than climatic causes, compared with plant diversity in which genetic exchange and speciation are considered driven more by climatic changes causing fragmentation and coalescing of vegetation types. Periods when montane vegetation was in contact with lowland vegetation may have been very favourable to genetic exchange and speciation. As a result of a fall in temperature montane ora moved to lower altitudes where it came into contact with lowland forest ora, and also migrations of montane ora could take place. Thus Mount Cameroun and East African mountains share 53% of montane forest species and 49% of montane grassland species. Periods of aridity could result in isolated refugia of forest types which, although this might lead to some speciation in adaptation to a drier climate, more likely means species richness indicates persistence of these refugia through long periods of geological time. Thus species richness is related to time. The complete disappearance of forest due to aridity seems never to have occurred because the rich and varied ora and fauna of African rain forest is incompatible with such complete disappearance, and forest taxa from the Eocene to the Miocene can be seen to be related to presentday taxa, implying such taxa persisted through the Quaternary (Maley 1996). Stebbins (1974) suggested less extinction in the benign environment of tropical forests may be the key to high diversity. Others have argued tropical forest oral richness lies not with differences in speciation, but simply that the relatively benign and constant tropical environment has provided more time for speciation to take place; or that niche ne-tuning perhaps through competition or predation should be more feasible in an environment buffered from climatic extremes. Yet others have emphasized the greater structural complexity facilitates niche differentiation. Thus intensive selection for narrow and specic adaptations could be a general feature of tropical forest speciation (Gentry 1989). Although it is now appreciated that tropical environments are strongly uctuating and dynamic, the amount of

1.8 Species Diversity

19

physiological stress imposed by rainfall uctuations is relatively minor compared with the winter extremes experienced in temperate zones. An example of how two tree species co-exist in the West African rainforest is provided by the canopy species Celtis mildbraedii Engl. and Strombosia glaucescens sp. which have overlapping distributions. The former extends into the drier forest, the latter into the wetter, and both co-exist over large areas. Both have shade tolerant seedlings and saplings. At Kade in Ghana Celtis is very abundant in the upper canopy, Strombosia less so, but among the saplings Strombosia is much more common, so how does Celtis maintain its high adult abundance? Swaine (1989) suggests because mortality is much higher in Strombosia in all size classes, but Celtis has a relatively low mortality. Thus the persistent high mortality of Strombosia demands a high recruitment base.

1.8

Species Diversity

The two areas with the highest concentrations of species and endemics, believed to be areas where the dense forest has survived past arid periods, lie either side of the present Congo forest block, in Cameroun-Gabon and the eastern DR Congo. Other areas are in west Africa and near to the east African coast. The forest ungulate fauna is less diverse than that of the savannahs with some 29 species of ten genera compared to 43 species of 28 genera, but on a local scale forest ungulate communities can be very diverse, including 16 co-occurring species although compared to 19 in the most diverse savannah areas. Overall, more species of ungulate have been recorded in African than in Asian or Neotropical forests. The 17 species of Cephalophus African duiker genus make it the most species rich group of forest ungulates known (Hart 2001). The eastern African mountain forests forming the Eastern Arc are of great age, their isolation and fragmentation combined with acting as condensers of moisture originating in the Indian Ocean since their original formation, comprising a moist habitat produce remarkably high levels of endemism and diversity with about 2530% of some 2,000 plant species in 16 genera endemic or near endemic to the forest and forest edge. Endemism is even greater in moisture-dependent amphibians, or forest-dependent invertebrates such as millipedes of which it is estimated there could be 1,000 endemic species in Tanzania, and of those in the Eastern Arc forests there are no genera in common with Congo-Camerounian forests while even differences between the montane faunas within Tanzania tend to be at the generic level (Hoffman 1993). These Eastern Arc amphibians and millipedes are both palaeoendemics, relicts of the former pan-African forest, and neoendemics, more recent immigrants which survived elsewhere. The more recent forests of the eastern Africa volcanoes have considerably fewer endemics, mostly neoendemics. Compared with western Africa forests the highly fragmented forests of eastern Africa appear to have fewer species overall but a relatively high proportion of endemics. The afnities of the ora are primarily with the Guineo-Congolian region of West

20

Africa Background to Exuberance

and Central Africa, but direct contact would have been severed with uplift of the central plateau at the end of the Miocene. Late Miocene climatic changes in southern Africa resulted in extinction of southern temperate forests, so the Eastern Arc forests do not have a signicant southern origin (Lovett 1993; Wasser and Lovett 1993). The Guinean zone lying north of the forest compared to the forest and the Sudanian zones to its north, is much less populated by humans and thus less disturbed. Why this should be so is not clear. One suggestion is that it forms a tsetse zone which inhibits cattle raising, another is that the soils are poor, and another, unlikely, that the population may have been reduced by the slave trade and has never recovered. Yet another suggestion is that the north developed in response to traders from across the Sahara, and the south to maritime trade from Europe, leaving the central zone undeveloped. With its higher rainfall than the Sudanian zone it should be more favourable for agriculture, but its capacity for regrowth perhaps may have been too great for farmers with simple tools (Lawson 1986). Tsetse y seems the most likely inhibitory cause to development, as it has been elsewhere in Africa.

1.9

Buttery Speciation

Forest butteries can be separated into Lowland and Highland divisions, the former divided into the Western Sub-division encompassing the main Guineo-Congolian forest region, and the latter the Eastern Sub-division of the East Coast forests. The latter is poor in species but most are either endemics or very distinct subspecies of genera which are much better represented in the western forests. Their distinctiveness suggests that broad-based connection between the western and eastern forests is ancient, probably of Miocene date. If more recent connections existed they must have been incomplete and probably by way of southern Tanzania. Distribution in the Western Sub-division is believed inuenced more by past forest refuges than present-day ecological barriers. That many forest butteries are represented by fairly distinct races in Upper Guinea, Cameroun, Gabon, east DR Congo, and Uganda, supports the concept of the equatorial forest contracting drastically during arid phases, possibly breaking up into limited forest refuge regions surrounding elevated areas of high rainfall. Four zones of the Western Sub-division are recognized (1) the Western Zone which includes the Guinea Forest Block and Western Nigerian forests with the Cross and Niger rivers marking the eastern distributional limit of many West African populations, poor in species but it has evolved a considerable degree of subspecic differentiation and a number of endemic species and (2) a Central Zone of Cameroun and Gabon and (3) DR Congo Zone, are very rich in species, the main centres of diversity lying either side of the Congo Basin, differences between the two zones being mainly at the subspecic level; (4) Uganda Zone, poorer in species than the Congo Zone, the eastern extremity represented by the Kakamega Forest being very impoverished.

1.10

Fish and Amphibian Diversity

21

Fragmentation of forests in Uganda, in contrast to southern DR Congo, has caused much peripheral subspeciation. Aubreville (1949) considered southern DR Congo to be anthropogenic, re-impoverished habitat, in which the tropical forest has been destroyed within recent times accounting for lack of subspeciation in its relic patches. The close similarity between montane buttery faunas is attributed to a former connection during moist and cool wet phases, but seven geographical zones are recognized (1) the Cameroun Zone, poor in species with few endemics and sharing some species with montane zones to the east; (2) Kivu-Rwenzori Zone, probably the richest in species with many endemics, attributed to its persistence as a refuge area; (3) Ethiopian Zone, poorer in species than the former and the Kenyan Zone but with a number of endemic species and many endemic subspecies due to isolation; (4) Kenyan Zone divided in two by the Rift Valley, with to the west an impoverished version of the Kivu-Rwenzori Zone, while to the east Mount Kenya and the Aberdares are more closely related to the Ethiopian Zone; (5) the TanzaniaMalawi Zone, separated from the Kenya Zone by a narrow strip of semi-desert north of Mount Kilimanjaro, has many endemic species and very distinct subspecies but the montane forests of Ngorongoro, Meru, Kilimanjaro, and the Chyulu Hills are much poorer in species than forests along the eastern edge of the tableland, including those of the Nguru, Pare, Uluguru, and Usambara mountains; (6) the South African Zone south of the Limpopo is characterized by its poverty and few endemics; while (7), the Angolan Zone, is insufciently known (Hamilton 1976) but has three known endemics.

1.10

Fish and Amphibian Diversity

Africa has more than 2,900 known species of indigenous freshwater shes, more than 28% of them endemic to the rain forest regions of central and west Africa. In the Congo Basin 669 species representing 25 families and 168 genera have been recorded, with 82% endemism at the species level and 42 endemic genera outside of Lake Tanganyika. In the central basin of the Zare River, 408 species of 24 families have been reported. The extraordinarily high level of endemism occurs in several of the coastal rivers from Nigeria to DR Congo also, but rivers draining the small forests of western Uganda are characterized by widespread species and low endemism (Chapman 2001). The rivers and lakes of nearly the whole of Africa north of 5 N share a similar and impoverished sh fauna known as the Soudanian or Nilotic. Endemic species are particularly numerous in West African rivers owing into the Gulf of Guinea indicating a greater maintenance of river ow than elsewhere. Of 115 species of Nilotic sh, 74 occur in the Niger River but 22 only are found in the Zare River. The Niger River resulted from two former rivers, the lower south-east owing section originating in the southern slopes of the Ahaggar Mountains from afuents which are now almost extinct. Lower down it joined the Sokoto and Benue. The Upper Niger owed north-eastwards from the mountains of the Guinea-Sierra

22

Africa Background to Exuberance

Leone border, then during the Late Pliocene and Early Pleistocene westwards into the Gulf of Senegal. A following arid phase produced a barrier of sand dunes which blocked the westward ow of the upper river. When the next wet phase arrived the river was diverted into a closed basin forming Lake Arouane which later drained away and the course joined the lower Niger about 5,0006,000 years B.P. Similarities of the Nilotic sh fauna to that of Lake Chad, the Niger, and Senegal rivers, may be due to extinction of a large part of the pre-Pleistocene Nilotic fauna during periods when the White Nile was not owing during the Late Pleistocene. A series of xed dunes extending from 10 to 16 N crossed the White Nile at one point probably causing the lower reach to dry up. A lower level Nile must have been seasonally much reduced and could not support so many species of sh. With resumption of higher ow in the Holocene more sh were able to exploit the river, mostly coming from well-watered regions of West Africa. This was facilitated by early Holocene wetness along the southern fringe of the Sahara and shifting dunes generating river capture over a generally at terrain. Zarean shes, although much closer, depended upon isolated accidents of tectonic, volcanic, and erosional river capture, and were unable to colonize the expanded Holocene Nile (Livingstone 1980). Richness of species and endemics in the Zare basin is indicative of persistence of river ow over a long period, the existence of a wide range of habitats, and prolonged isolation. The sh faunas of Lakes Victoria, Tanganyika, and Malawi, are dominated by cichlid species exhibiting astonishing levels of speciation and endemism. Lake Tanganyika has 247 known sh species from 19 families, Lake Malawi 242 species from nine families, and Lake Victoria formerly had more than 238 species from 12 families (Lowe-McConnell 1987). Cichlids comprised 84% of species in Lake Victoria, 82.6% in Lake Malawi, and 55.1% in Lake Tanganyika. The species ock of rocky shore cichlids in Lake Malawi have evolved over only the last 200300 years, related to changing lake levels between 1500 and 1800 (Owen et al. 1991). Possible recent losses due to persistent poisoning with insecticides, as in CAR, are unknown. Rivers in the heart of Africa have been impoverished of both sh and invertebrates to an unknown extent due to the practice of pouring insecticides into the rivers to kill sh for consumption (Spinage 1988). As to amphibians, some 10% of the worlds known species have been reported from Camerouns rain forests, while with 28 species Tanzania has the richest Bufonid fauna in sub-Saharan Africa (Lawson and Klemens 2001).

1.11

Bird Diversity

The most remarkable Family of plains birds of Africa barring none Chapin (1932) considered to be the ostrich Struthio camelus. Not restricted to Africa, the Family occurs in south-western Asia also. It is unknown in the West African forest subregion and the Congo, and in equatorial Africa occurs on the dry plains of the east only, otherwise being characteristic of the arid regions of both northern and

1.11

Bird Diversity

23

southern parts of the continent. As a ightless bird Chapin believed it must have become so by isolation on an island where there were no predators, probably in the Mediterranean region. He concluded todays faunal relationships of birds in Africa were largely determined by past continental connections, past climate, and topography, present climate and topography determining the ranges of living birds largely through their inuence on vegetation and by the cooler temperatures on mountains. Bird species of recent radiations are found generally in savannahs rather than in forests. Within the forests, montane forests such as those of the Rwenzori-Virunga area are more signicant for species origination than lowland forests which tend to be areas of species accumulation. The Usambaras, Ulugurus, and East Uzungwas have the highest diversity and endemism in montane forest birds compared with African montane avifaunas as a whole, one of three main centres of endemism on the continent, the others being the Albertine Rift and Cameroun. The bird fauna is rather homogeneous throughout the lowland forests of West and Central Africa with 86% of species recorded from the Guinea Forest Block found also in north-east DR Congo, which has some 212 species. Only nine species are endemic to the Guinea Forest Block and many of the species around Lagos are subspecically identical to those in Guinea forests. Similarity with the Guinea Forest Block decreases from west to east across Nigeria. Moreau (1966) concluded that in West Africa old interruptions in the forest were more decisive in forming the modern distributional patterns than present gaps. Six endemic species of lowland forest bird are conned to north-eastern DR Congo, and a further 24 species show disjunct distributions within West and Central Africa, which seems to support the existence of former lowland forest refuges on the western and eastern anks of the Zare Basin, but not for a refuge in its centre (Hamilton 1976). With a single exception, the bulbul Phyllastrephus hypochlorus, all birds of the lowland forests east of the Albertine Rift in Uganda, Southern Sudan, and western Kenyas Kakamega Forest, belong to species and subspecies found in DR Congo to the west of the Semliki River. But lowland forest in Uganda is impoverished compared with that of DR Congo, containing about half the number of species. In the East Coast forests 38 species only are found, of which seven are widespread some occurring as far south as the Cape. Some show well-marked disjunctions with the Congo Forest Block, and three or four are considered specically distinct from their relatives in the west. Moreau (1963) considered this East Coast bird fauna provided evidence of a former connection, perhaps on two separate occasions, with the main Guineo-Congolian forests. The montane forest birds of Cameroun, east DR Congo, Kenya, Ethiopia, Angola, Tanzania-Malawi, and south of the Zambesi (Ethiopia and Southern Africa apart), however widely separated colonized an already integrated community, rather than by a process of random long-distance dispersal as on oceanic islands. Moreau (1966) thus envisages contact occurring when climatic conditions produced one great block, much of it forested, extending from Ethiopia to South Africa, with an arm reaching across to Cameroun. But important differences between numbers of species and endemics in the different highland areas suggest differences in the environmental histories both

24

Africa Background to Exuberance

of the regions themselves and of their intervals, while a decrease in temperature is insufcient in itself to allow spread of montane forest, increase in humidity is required also (Hamilton 1976). Chapin (1932) considered the distribution of birds in DR Congo was to a great extent determined by the vegetation, but Wildeman (1940) asked whether it was the vegetation which determined the nature of the fauna, or if the fauna did not determine, at least in part, the constitution of the vegetation through seed dispersal, pollination, and changes wrought by man? One of the most striking but little investigated features of the ecology of the African continent is its population of migratory birds, which impose an enormous annual uctuation in the consumption of resources. Apart from migrations of resident birds within the continent there are many annual migrant Palaearctic birds, spending the northern winter in Africa and summer in Europe. Moreau (1972) estimated altogether some 283 species migrated from the West, Mid, and East Palaearctic, the majority, 179, from the West. Passerines other than warblers were the most numerous with some 85 migrant species. Hence each year about onefth of the non-forest birds in Africa are immigrant species, and more winter north of the equator than south of it. None of the migrants is purely frugivorous and only a small proportion wholly or mainly granivorous, the majority being dependent on arthropods as food. Only a few species travel via the Nile valley, many ying north or south on a broad front resting where they can but ying non-stop over the Mediterranean and Sahara. Some use different routes for the spring and autumn migrations. Flights may be up to 6,00010,000 km in length, from Tomsk, Yakutsk, and Lake Baikal, to Nairobi and southern Chad. The crossing of the Sahara when accomplished diagonally may involve a journey of up to 2,200 km and take 5060 h. North and south on most lines the distance a bird must y is 1,500 km and the energy requirements must be met by fat deposits accumulated before departure. One of the longest routes is from Yakutsk in Siberia to Nairobi, a distance of 10,000 km (Fig. 1.8). Birds taking this route can pick up food until south of Tomsk where they must cross 1,500 km of trans-Caspian deserts, unless they y east of the trans-Caspian deserts where they must pass the worst of the Arabian deserts over a distance of some 1,200 km. Those which y over the Mediterranean may have to cover 1,100 km non-stop followed by 1,600 km over the Sahara. Birds which say travel 6,000 km from near Tomsk to Khartoum, require twice the energy reserves of those which cross the Mediterranean and Sahara, and it is not known where they could replenish resources on the journey. Moreau estimated 4.3 billion passerine birds migrated each autumn from the western and central Palaearctic to Africa. Non-passerine migrants are estimated to number at least 200 million, while raptors total 40 million. The European stork Ciconia ciconia alone at one time totalled 700,000. The number of aquatic birds migrating is unknown. It is estimated also that half of all these migrants may perish on each journey, thus the numbers returning to Europe in spring are smaller than those departing in the autumn which have been reinforced by the new generation. Annual survival rates of sedge warbler Acrocephalus schoenobaenus, willow warbler Phylloscopus trochilus, and sand martin Riparia riparia, increase with the

1.11

Bird Diversity

25

Fig. 1.8 The Great Circle routes from Asia to Africa of some migrant birds. Cross-hatched areas show winter and summer ranges of the farthest travelling migrant, Little Stint Calidris minuta (Based on Moreau 1972)

increasing amount of rainfall in their western African wintering areas, and reproductive output can be lowered following a year with adverse wintering conditions (Schaub et al. 2005). Moreau estimated also that the West Palaearctic region due to loss of woodland to agriculture now accommodates about a quarter of its former potential population of woodland migrants subsequent to recovery after the nadir of conditions 18000 B.P. caused by the last glaciation, meaning a 75% reduction of demands on African resources. Aquatic bird numbers, which will have been less affected by the glaciation, have declined drastically over the last 2,000 years so that their demands on Africa are lower now than they have ever been. The migration of most species and its various patterns must have evolved only between about 15000 and 5000 B.P., and again in the past 5,000 years, and their

26

Africa Background to Exuberance

adaptations to this end Moreau sees as the product of evolution of about the last 10,000 years. However they may have been pre-adapted to the requirements of migration. African plains herbivores build up accumulations of fat which are exploited at the very end of the dry season if needs be. If it rains before this the fat is rapidly metabolized presumably as the animals have no need of it. Birds may have similarly evolved to build up seasonal fat deposits to withstand the dry season/ northern winter and simply adapted their use to fuel migration. Previously they may have made relatively short south-north, northsouth seasonal displacements within Africa, but as the cold region retreated further and further north, so their annual displacements were extended farther and farther as they took advantage of the new resources increasingly opening up to the north. Such a system would take only as long to develop as it took for the warmer temperature zones to extend northwards. Its rigidity, a simple involuntary increase in the travel distance each year rather than exploratory ights, is attested by the pin-point recurrence of species in successive seasons in identical sites in winter quarters. Most species appear to form small populations which breed in the same limited area and follow the same migration route to winter in the same area. Far less food is available for migrants north of the equator than south of it, but many more maintain themselves in the belt just south of the Sahara than south of the equator. Even within the northern tropics the number of species diminishes from north to south as the environment becomes more humid. This annual inux of millions of extra birds does not seem to cause undue competition with resident birds, but we do not know if the latters numbers are depressed as a result of it. However the warblers, for example, use different habitats varying their choice within even a small part of their African ranges, but lark subspecies are not segregated while in Africa and some migrant buntings seem to be in competition with both local and immigrant larks. One immigrant bunting has been shown to associate with a local bunting, presumably exploiting the same food. But breeding and initial growth being already accounted for, immigrants maintenance demands in Africas warmer clime are only some 60% of those required in the Palaearctic. Although the losses during migration are considered to be great, one yellow wagtail Motacilla ava in Nigeria was recovered for seven seasons (Moreau 1972). Until 1968 the whitethroat Sylvia communis was an abundant and widespread summer visitor to Britain and western Europe with a stable population. In 1969 the number of migrants decreased by 70% and uctuated around their lower level until the mid 1980s, since when a shallow recovery occurred. The loss of millions of this bird was due apparently to high mortality in their wintering quarters in the western Sahel, annual uctuations in abundance correlating with overwinter survival. Other trans-Saharan migrant warblers such as garden and willow warblers, have shared similarly timed population changes, while sedge warbler and chiffchaff declined earlier, in the late 1960s to early 1970s (Siriwardena et al. 1998). It has been pointed out with respect to birds, perhaps the most well known vertebrates in Africa, that many parts of the East Coast Escarpment in Tanzania are yet to be explored. Almost nothing is known of the northern extension of the Nguru Mountains west of Handeni, nor of the Rubeho Mountains, the Uvidunda

1.12

Mammal Diversity

27

Mountains, most parts of the Uzungwas and most parts of the Southern Highlands. Mountains lying outside of the main escarpment, such as Malundwe, Mahenge, Mabarika Mountains, Matengo Highlands, and the Njesi plateau in Mozambique, are equally little known. If this applies to the avifauna, how much more so must it apply to other groups, both vertebrate and invertebrate?

1.12

Mammal Diversity

The forests provide a substantially homogeneous environment at present but only 30% of forest mammal species are found throughout the main Guineo-Congolian forest region. There are far fewer species in the East African forests than in Central and West Africa and the small number of species in common suggests only a few versatile or mobile species traversed tenuous bridges between these regions, or that exceptional genetic stability has been maintained in disjunct populations over long periods of time. Kingdon and Howell (1993) consider it probable the East African forest fauna developed piecemeal over a very great and unknown period of time and that by no means all of its members derive as immigrants from the lowland forests of the Congo Basin. Lnnberg (1929) suggested a more or less continuous forest o once stretched across equatorial Africa and now only scattered remnants remained, isolating animals such as the potto Perodicticus potto, giant forest hog Hylochoerus meinterzhageni, and bongo Tragelaphus euryceros. He further suggested rain forest once covered the greater part of Africa, and as it shrank during the Miocene the continent was invaded from the north-east by a fauna from Eurasia, including numerous species of antelopes, buffaloes, giraffes, equids, rhinoceroses, and even aardvarks, leaving island faunas in the isolated forest relicts which led to differentiation of species and races. But the savannahs are inhabited also by animals descended from forest dwellers, species such as ground squirrels Xerini and red monkey Cercopithecus (Erythrocebus) patas, which survived the disappearance of much of their habitat and competed successfully with invaders. Speciation even of plains fauna may have been favoured by isolation through periodic forest extension, and also by large rivers like the Tana and Zambesi separating populations. There are three mammalian main centres of endemism: Liberia, GabonCameroun south of the Sanaga River, and east DR Congo in the Ituri-Maniema region, which may have been sites of forest refuges during arid Pleistocene intervals. The mammal fauna of Liberia is rather poor in species probably having been largely isolated from the Congo Forest Block its probable origin. East DR Congo has the most number of species perhaps because it was the largest and ecologically the most varied, and because of its central position. The number of species of forest mammals decreases regularly from the Ituri River eastwards to the Indian Ocean. Kingdon (1971) considered there were two colonization routes from west to east: across Uganda to the Kenyan highlands, and south of Tanzania to the coast. Mammals in forest on the northern route are generally indistinguishable from those in east DR Congo, implying recent spread. The southern route contains some

28

Africa Background to Exuberance

endemic species and most of the remainder are subspecically distinct from those of the northern route, suggesting spread from the west followed by a barrier of long duration. These two routes meet approximately between the Usambaras and Mount Kilimanjaro, with some overlap to the north of this line. Although savannahs carry a higher biomass of vertebrates than the tropical forest, studies have shown that although variability exists some areas of tropical rain forest can support a large mammalian biomass. In one area of former logging in Lope, Gabon, biomass has been estimated at almost 6,000 kg/km2, mostly accounted for by elephants (White 1994). But if we remove elephants from the equation, the residual mammalian biomass is remarkably constant, averaging 626.5 kg/km2 over ve study areas (range 480.6691.7). This compares with the highest savannah estimates of more than 30,000 kg/km2 in the Virunga NP of DR Congo where hippopotamus were not present, and up to over 180,000 kg/km2 at high hippopotamus density; while temporary associations of grazers composed of warthog Phacochoerus aethiopicus, buffalo Syncerus caffer, kob Kobus kob, waterbuck K. defassa, and topi Damaliscus lunatus, on fresh ush after burning have reached more than 200,000 kg/km2. This large number and variety of grazing herbivores, the variety inuenced by the plant forage standing crop, is one of the most striking features of African ecology. Forage quality may decrease with increasing plant standing crop and with maturation thus reducing the net nutrient and energy intake by grazers. Large grazers are better able to convert high biomass/low quality forage than are smaller species and thus decrease the standing crop thereby improving the quality and leading to facilitation for smaller grazers unless the difference in body size is too great, then large grazers may keep the vegetation at an equilibrium which is of too low quality for smaller grazers. When grazers are of similar size competition may ensue, but coexistence may result from variation of the standing crop between years due to climatic uctuation. Prins and Olff (1998) demonstrated that these factors impose a certain regularity on body size, each species on average being an assemblage with a constant weight ratio, that is, it is larger than the next smaller one in constant proportion. During the Late Pleistocene the Palaearctic, South American, and Australian mammal faunas underwent massive extinctions. South America lost some 76% of all herbivore genera heaver than 5 kg, North America 75%, and Europe 45%. But Africa lost 13.5% only, retaining its full diversity. Large body size permits wide scale foraging for high-volume harvesting and mechanical advantages for removing and macerating plant tissues and development of systems necessary for digesting low quality food. When digestibility decreases gross intake rate is reduced because the food takes longer to digest, thus a larger gut is required to obtain the required amount of conversion. The metabolic rate, the rate at which energy changes take place in the body, is a regular function of body size and close to the power of 0.75. Thus for every unit increase of mass the metabolic rate decreases by one quarter. Hence the energy turnover of an elephant weighing 4,790 kg is approximately equivalent to that of ve buffaloes, or ten wildebeest Connochaetes taurinus, or 29 impala Aepyceros melampus, or 150 dikdik Madoqua sp. Coupled with their large size the high mean survival age of elephants can make relatively massive interventions in terms of diversion of energy ow in an ecosystem.

1.12

Mammal Diversity

29

The crude protein content of grasslands decreases at high biomass, decrease being greater on nutrient poor soils than on nutrient rich ones. The only way small herbivores can use a low quality food as in high plant biomass is either by a low intake with a long digestive time, or by a high intake with a high passage rate. In both cases the net daily intake rate per unit body mass will be low, but the food intake per unit body mass decreases with increasing body mass. At low vegetation biomass smaller grazers have a competitive advantage over larger ones because of their higher intake per unit of body mass, but at higher vegetation biomass they may need facilitation by larger herbivores in order to achieve their intakes. Removal of the high biomass vegetation increases the quality of the vegetation to a level where it can be used by smaller species. Species richness of grazers is highest at intermediate primary productivity levels where facilitation interactions are strongest. Only if an ecosystem is unfragmented and greater than about 12,000 km2 in area, unaffected by human changes and stochastic processes, is competition unlikely to be the cause of species loss. In large enough areas population densities will be sufciently high to prevent population extinctions in adverse periods, and the number and area of different habitats will probably be large enough to prevent too much niche overlap. Species analysis suggests a gap in the numbers of mammals greater than 1,000 kg mass expected in grazer assemblages, estimated at six to ten. Although Africa experienced few extinctions of large herbivores at the end of the Pleistocene a number went extinct before this: four elephant species, Elephas recki, E. iolensis, E. zulu, Loxodonta atlantica, about 400000 B.P.; a giant hippopotamus Hippopotamus gorgops and giant hartebeest Megalotragus priscus 12000 B.P.; and giant buffalo Pelorovis antiquus 4000 B.P. (Owen-Smith 1988); totalling seven known species. Coe (1981) argued the larger animals are unable to match recruitment with a high hunting pressure, and life history strategies evolved over a long period of time may have made them more susceptible to comparatively low levels of harvesting. The removal of between 5% and 15% of the standing crop biomass each year would have exceeded production by a level beyond which recovery becomes impossible and local extinctions could take place in as little as 100 years. Against this we have to consider the vast area of forest open to these animals and the low densities of early man. Is the surviving elephant that more dangerous, that more adept at outwitting hunters, that it survived? Or is its survival due to its wide range of herbivorous diet and method of exploiting it, from grass to trees, which would have ensured survival when a more stenotypic diet would have failed it? Is the giraffe an anomalous survivor of hunting pressure, or has it survived because it is adapted to life in a semi-arid environment and thus withstood the vicissitudes of past climate? Distribution of species across the continent is not equal, a reection not only of the vegetation but of evolutionary history and mans historically recent disturbance. Analysis of grazer species richness of 96 species shows the highest numbers occurring today in the savannah of northern Tanzania and Kenya in East Africa, and in the Lowveld border area of southern Zimbabwe, southern Mozambique and northern South Africa (Fig. 1.9); all areas of intermediate primary productivity. Species richness in the Guinea savannah of West Africa, characterized by high

30

Africa Background to Exuberance

Fig. 1.9 The regions of highest animal species diversity (After Prins and Olff 1998)

grass productivity and low quality, is much lower. Resource competition between grazers of approximately the same size is potentially a strong factor shaping herbivore assemblages and thus the smaller an area the less likely is co-existence possible, while the difference between the smallest and the largest grazer in the system also dictates species richness, large grazers requiring more vegetation biomass, hence more area, to satisfy their requirements, but which in turn at high primary productivity levels facilitate exploitation by smaller species.

1.13

Herbivore Community Organization

Allee et al. (1949), with particular reference to grassland communities, illustrated how stratication is a principle of organization of the community. Grasslands have three vertical strata: subterranean, oor, and herbaceous. Insects are among the

1.13

Herbivore Community Organization

31

most abundant occupants and rodents are prominent among mammals. The subterranean level is particularly important, partly due to the seasonal aridity of the above ground habitat and the relatively slight protection afforded by grassland to high day temperatures and high light intensity as contrasted with forest habitats. The grassland oor has less bulky leaf mould compared to the forest oor, but may have a high, or higher, humus content in the soil. Allee et al. compared the stratication of vertebrate species in grassland communities among the different continents, showing that although there were equivalents in most categories among all continents, Africa was richest by far. Beginning with the subterranean stratum it is represented by fossorial herbivorous mammals such as the African ground squirrels Xerus spp., and a saltatorial herbivore the springhare Pedetes capensis with a niche in the subterranean oor stratum and feeding niche in the herbaceous stratum. They are followed by the golden moles Bathyergidae. The ostrich is a cursorial bird with a habitat niche on the oor and feeding niche on both oor and herbaceous strata. It is followed by the cursorial herbivorous gregarious mammals, also with a habitat niche on the oor and feeding niche in the herbaceous stratum, illustrated by the zebra Equus quagga and some 30 genera of antelopes and gazelles. Cursorial predators with habitat and feeding niches on the oor stratum are divided into snakes and mammalian carnivora. In the former category are the puff adder Bitis arietans, black-necked cobra Naja nigricollis, and python Python sebae. Mammalian carnivores are represented by hunting dog Lycaon pictus, serval Felis serval, caracal F. caracal, cheetah Acinonyx jubatus, and lion Panthera leo. There is also both a diurnal and nocturnal separation. The herbivorous mammals are responsible for at least three widespread biotic effects. Firstly the presence of predators in sufcient numbers to maintain a biotic balance with their food supply. The extent to which they might regulate the herbivorous population is questionable, any depressant effect is more likely to be upon the neonatal cohort than the adult cohort, but the predators are in turn regulated in part by abundance of their prey. In part because, if a prey species became adept at avoiding its predator it would not matter how abundant it was if the predator could not catch it. The predators include amphibians, reptiles, birds, and mammals, feeding chiey upon insects, rodents, and ungulates. The rich grassland herbivore population of Africa is parallelled by an equally rich predator population. By comparison, in Australia the plains have fewer native predators and fewer large native herbivores, the marsupial population having radiated and ourished in the absence of effective competition. The second effect of herbivores is the contribution to the invertebrate life of the subterranean and oor strata by dung feeding coprophagous insects. Notably scarabeid beetles and numerous ies which oviposit in the dung upon which their larvae feed. Mature and immature scavenger ies and beetles are important in transporting coprocolous bacteria and numerous larval, nymphal, and mature mites and parasitoid Hymenoptera. Finally, the grassland oor herbivores through their dung fertilize the herbaceous stratum, affecting regulation of plant growth and plant nitrogen xation.

32

Africa Background to Exuberance

In addition to these effects, heavy grazing, as occurs with the dense concentrations of herbivores in Serengeti, stimulates plant productivity. Experiments demonstrated that net above-ground primary productivity of grasslands was strongly regulated by grazing intensity in wet season concentration areas, moderate grazing stimulating productivity up to twice that of ungrazed controls, depending upon soil moisture. Productivity was maintained at control values even under very intense grazing, questioning the concept of overgrazing, and the high grazing load of the Serengeti ecosystem has seemingly constituted strong selection on the plants for compensatory growth upon defoliation (McNaughton 1979). Sinclair (1975), studying the effect of large herbivores on the grasslands of the Serengeti, was one of the few to look also at the effects of small mammal and some invertebrate consumers, but in deducing that they all contributed to maintain an apparently stable system overlooked the probable past effects of aperiodic locust invasions. He considered invertebrates and small mammals were 45 times more efcient at converting primary production to animal protein, ungulates having a conversion rate of some 0.4%, compared with 1.5% for grasshoppers assuming a production to biomass ratio of the latter of 3:1. He recorded some 38 species of grasshopper in the Serengeti grasslands, of which Mesopsis abbreviatus, Coryphosima stenoptera, Afrohippus taylori, together with, Rhaphotitha spp. and Acrida spp., made up more than 80% of the long grass population. In the short grass areas A. taylori, Dnopherula backlundi, Acrotylus elgonensis and A. patrualis were dominant. In the long grass areas in the dry season the mean total requirements for food by herbivores was always in excess of the available food, some 95% of the demand being from the ungulates. The grasshopper population component of the invertebrates fell due to reduction of habitat through burning and through grazing by ungulates, cessation of breeding, adult diapause, and mortality, thus contributing very little to consumption at this time of the year. But when they built up in numbers in the wet season their impact must have been at least equal to, if not greater than, that of resident ungulates. Small mammals remained low in numbers throughout the year. On the short grass areas throughout the dry season there was practically no green food and the invertebrates required more than all the mammals, which were a few hares Lepus spp., Thomsons gazelle Gazella rufrons, and oryx Oryx beisa. In the wet season migrant ungulates accounted for more than 90% of consumption, resulting in less available food and a smaller number of invertebrates. In the rock outcrops where there was little offtake by the ungulates, there was a higher population of grasshoppers but small mammal offtake was four times that of the long grasslands due to the higher rodent populations and presence of hyrax Procavia, but demand was in excess of production for only 1 month of the year. While ungulates consumed a signicant proportion of dry material this did not mean it could be assimilated as food. Both Orthoptera and rodents preferred green grass which was the limiting resource in the form of protein. The browse resource was also limited, lepidopteran caterpillars fed only on new leaves of trees and bushes, ungulate browsers also rejecting mature leaves for although green the leaves contain buildups of tannins.

1.14

Parasites and Diseases

33

Only a few of the 36 or more species of rodent recorded from Serengeti were dominant in the grasslands. In the long grass areas the dominant species were the grass-eating swamp rat Otomys tropicalis and multimammate rat Mastomys (Praomys) natalensis. In the short grass areas there were a few springhares P. capensis and African hares, with smaller rodents scarce, but the grass rat Arvicanthis niloticus and swamp rat were present. The corollary of this is that a signicant decline in the large herbivore populations could result in explosive population numbers of rodents and phytophagous invertebrates.

1.14

Parasites and Diseases

Diseases are likely to have played a large part in the generation of the immense variety of plants and animals in the tropics. This growing variety has in turn driven evolution of disease diversity (Wills 1996). As with so many things Darwin said it rst. Thus with epidemic diseases, When a species, owing to highly favourable circumstances, increases inordinately in numbers in a small tract, epidemics at least, this seems generally to occur with our game animals often ensue; and here we have a limiting check independent of the struggle for life. But even some of these so-called epidemics appear to be due to parasitic worms, which have from some cause, possibly in part through the facility of diffusion amongst the crowded animals, been disproportionately favoured: and here comes in a sort of struggle between the parasite and its prey (Darwin 1859). A parasite population is generally characterized by a higher intrinsic growth rate than that of its host, while a predator generally has a lower intrinsic growth rate than its prey and may use several different prey species, in contrast to parasites which tend to use one host (Dobson and Hudson 1986). The essential difference between a predator and a disease is that a disease is a microparasite which feeds and reproduces inside the body of the victim. A virus can multiply only while the host cells are living, but rickettsias (small, intracellular bacteria) reproduce maximally when the cells are effete. A macroparasite reproduces outside of its victim but may feed inside it and may be likened to a predator, but a predator sensu stricto consumes the victim, or parts of it, from the outside. In Grubbs analysis (2001) of rain forest mammal distributions, and with reference to other phyla such as Amphibia, no consideration is given to the possibility of foci of diseases and parasites fragmenting distributions. It is not necessary to invoke epizootics, although these could equally have played a role, but centres of origin of enzootic diseases or parasites could well determine faunal distributions on the smaller scale, especially in forests, where for example, the susceptibility of primates such as chimpanzee to epizootics of certain arboviruses is established. Equally, climatic uctuations could have caused elimination by diseases of plant species in dened areas, such as moulds which ourish in warmer conditions or affect plants when they are stressed by drought. Diseases have been isolated

34

Africa Background to Exuberance

globally since the Pleistocene making them often fatal when brought into contact with new but related hosts. An example is provided by the elephant endotheliotropic herpes virus benign in the African elephant but fatal to the Indian. Had the land masses not separated between the Mesozoic and Tertiary Eras then there would have been less diversication of life today and pathogens would have evolved, destroyed, and been adapted to, host populations worldwide, except where conditions for life were too extreme. Thus the present diversity is in a sense articial, the result of geological tectonics not biological processes. If a disease now spreads into a new continent it is only doing what it might otherwise have done had continental drift not taken place. A traditional view of parasites and diseases is that they are normally benign specialized predators living in balance with their hosts, and epizootic mortalities are cases where environmental factors have disturbed this tenuous balance. It was rationalized that parasites were unlikely to have an effect on host population dynamics because if they led to death of the host then the parasite would die also. But the lifetime reproductive success of a parasite does not depend upon survival alone, rather on the interactions between survival, reproduction, and transmission, which determine the parasites ability to establish reproducing offspring in new hosts (Tompkins et al. 2002). Diseases or parasites are generally neglected in the study of ecology in favour of the predatorprey reaction, whereas, broadly dened by Anderson and May (1991) to include viral, bacterial, protozoan, and fungal pathogens, together with helminth parasites, they play a more important role than predators in the regulation of the numerical abundance and geographical distribution of animals. An example of the complexity of disease interactions comes from Belgium where increased seed production of trees resulted in an increase of bank voles Clethrionomys glareolus which spread in their urine more Puumala hantavirus infective to humans, causing a rise in cases of the kidney disease nephropathia epidemica (Escutenaire et al. 2000). Hobley (1932) stressed the importance of disease in wild animals at an early date and Bodenheimer (1938) included diseases as one of the biotic factors in biological equilibrium, together with food, population density, and the reaction basis of the organism, and parasites are now seen to operate in a density-dependent manner like predation. Thus they may serve to regulate the density of a species, unlike the more traditional view of pathogens which tended to consider them as operating infrequently in a more random, density-independent manner. May (1982) acknowledged the fact that parasitic infections, which include diseases, may exert a role in regulating animal populations. While most research has been devoted to exploring the roles of competition or predatorprey interactions, parasitic infections may exert much greater inuence. A classic example is the increase in wildebeest and buffalo populations in East Africa after rinderpest was controlled, the populations then becoming limited by the food resource. The relationship may be more complex, effects of parasites interacting with those of predators, weather, and intra and inter specic competition. Thus predators which chase their prey, such as hunting dog, cheetah, and lion, may prey on the more heavily parasitized individuals either by conscious selection or because the victims simply do not run as fast as the

1.14

Parasites and Diseases

35

others. The downside is that the predators themselves may become more heavily parasitized in cycles where they form the intermediate host. A leopard Panthera pardus ambushes its prey so it has no effect upon reducing the more heavily parasitized members of a population. Weather affects parasite transmission rates through inuencing vector activity and distribution, as well as directly affecting disease transmission. It can cause stress in a parasitized host also allowing the parasite burden to increase. Multiple species keep down parasitism and disease by interrupting transmission from one susceptible host to another, and parasite-stressed individuals are likely to fail in competition with less affected members of the same population. High density populations tend to have increased parasitism because transmission of the parasite from host to host is facilitated and the hosts become less resistant through interspecic competition for food. Holmes (1982) argued parasites do not generally regulate host populations but that any mortality caused is compensatory, replacing other mortality. Africas rinderpest panzootic was an exception, being ostensibly an introduced disease it was additive, operating in addition to other mortality. However once it became enzootic among the cattle population its role became compensatory according to Holmess interpretation. Although the term yearling disease was applied to the annual mortality of wildebeest calves by rinderpest in Serengeti from the 1930s, seasonality in wild life diseases in Africa is a neglected study. Seasonal components most frequently arise from changes in host behaviour through the year. Increased transmission may result from more contact at waterholes during the dry season, from reproductive behaviour, and from migrations. These factors can increase the contact rates between susceptible and infectious individuals while the behaviours can cause stress and weakening of resistance in individuals. Allan (1965) considered one must reasonably suppose primitive human populations tended to decrease on exposure to, among other things, debilitating diseases, and to increase rapidly under favourable conditions; pointing out that tendency to increase has predominated in the long run such that man has spread into almost every habitable corner of the earth accessible to him, we might say Africa, even into regions on the very margin of habitability. Moss (1969) was one of the few also to consider diseases in an ecological context, noting, Any evaluation of the ecological background in Africa must necessarily include some mention of the ecology and importance of the many organisms which cause pathological symptoms in human beings, listing the 21 most common diseases. Apart from the direct pathological effect, they exert an indirect effect also in determining spatial distribution. Thus river valleys, although usually the most fertile areas in a landscape, frequently harbour disease carriers and vectors. Allan (1965) suggested this may be at the root of some tribal legends and may discourage also regular wet and dry season migration. Viruses are the largest taxonomic group of emerging plant pathogens. Ridley (1930) wrote, When plants are too close together, disease can spread from one to another and become fatal to all. Where plants of one kind are separated by plants of other kinds, the pest, even if present, cannot spread. Haldane (1949) suggested

36

Africa Background to Exuberance

infectious agents might be very important in the maintenance of genetic variability and even may have played a role in the evolution and maintenance of sexual reproduction. Sexual reproduction persists because it enables many species to rapidly evolve new genetic defences against parasites that attempt to live off them and it also purges mildly deleterious genes, which is a key advantage if mutations in interacting genes are more deleterious in combination than expected from their individual effects. Natural selection can more easily purge deleterious mutations by means of sexual reproduction (Azevedo et al. 2006). Gillet (1962), discussing tropical forest trees, dismissed the idea it was a multiplicity of small niches which accounted for the multiplicity of species but pest pressure, pest meaning any sort of minor predator, parasite or herbivore, such as fungi, bacteria, and invertebrates, which prey upon an organism much bigger than themselves, generally referred to now as pathogen pressure. Pest pressure is the inevitable, ubiquitous factor in evolution which makes for an apparently pointless multiplicity of species in all areas in which it has time to operate. He continued, The answer to a problem which has been discussed by Haldane, why each species does not come to consist of a single genetic type, that most suited to the environment, is also plain: the effect of pest pressure in producing genetic diversity applies at the intraspecic as well as the specic, genetic and family level. That strain within a species which is commonest is the one to which the pests of that species will tend to become most adapted, therefore the viability of this strain will be reduced and other forms will be favoured. Predation, he suggested, can be a powerful motive force in evolution because it can make the environment more diverse for the species being preyed upon, and thus produce an even greater variety of ecological niches. Could Gillets hypothesis explain the inordinate diversity of beetle species? Beetles are primarily detritus feeders, a food source which exposes them to a rich array of bacteria and viruses. Those Orders exhibiting few species are composed of selective feeders, and although such species may pick up fungal and other infections in passing, diseases picked up from a food source will be limited. In forests, or in animal colonies or herds, non-immune individuals are protected by being surrounded by immunes which prevent the pathogens from spreading and multiplying to high numbers, termed herd-immunity. If a species of tree in a rainforest becomes too common its pathogens will increase in number as well, soon spreading outwards. This drives down the numbers of that species of tree leaving room for other tree species to supplant them, and when these become so numerous that their pathogens can spread then they too are driven down in numbers and the pathogens act to maintain different species of tree within a forest. Thus diseases play a large role in shaping the diversity of living things (Wills 1996). Gillet used the example of the succulent shrub the Desert rose variety Adenium somalense Balf. f. at Dandu in northern Kenya. Apparently well-adapted with its poisonous sap to withstand grazing in arid regions it was nowhere abundant although occurring over wide areas as scattered individuals, or in small clumps. Gillet found almost all fruits he collected were infested by ovule-eating larvae of the y Dacus brevistylus. Thus, he postulated, had the host plant been more numerous the y also would have been more numerous and would have found the plant more

1.14

Parasites and Diseases

37

easily, thus damaging more of the seeds and the plant would have become scarce again. Pest pressure would be expected to be most obvious in those regions where conditions have been stable the longest and it is there that one nds the most diversity, for example among the Cape ora, and least in driest areas where there are less pests. In Tanzania it has been shown that when new ground is taken into cultivation for sugar cane the latter can be devastatingly attacked by a Melolonthid chafer Cochliotes melolonthoides, formerly considered to be a forest insect. Gilletts hypothesis does not seem to have received support although Burdon (1987), while not referring to Gillet, noted the central role that pathogenic organisms potentially have in inuencing the ecology and evolution of individual taxa and the composition of plant communities in which they occur. But although most mechanisms for introducing new taxa, immigration, hybridization or in situ speciation, would be independent of pathogens, Burger (1992) noted pathogen pressure could facilitate the process under some conditions. But it is apparently ignored, for example, by Gentry (1989), although Ashton (1989), without reference to Gillet, suggests plant population densities (and thus competition and speciation) may be inuenced by insect herbivores, seed predators, pathogenic microorganisms, and allellopaths, while the chemical arbiters of ectotrophic mycorrhizal symbioses may determine the modes of soil resource use. Hamilton (1982), apparently unaware of Gillets work, suggested the effect of parasites on genetic diversity may be vast. Parasitism caused not only arrays of varying traits concerned directly with disease resistance, but also the evolution of meiosis itself setting up the basis of all Mendelian variation. In other words it was the rationale for sex, species evolving to exclude parasites as Haldane had suggested. Under pathogen pressure sexual reproduction may be favoured because it maintains genetic diversity and production of rare genotypes. Outcrossing and recombination allow for production of rare offspring (genotypes) that are expected to have a greater chance of escaping parasites (Lively 1996). Clay et al. (2008) state that host-specic pathogens are more likely to attack and reduce population sizes of common relative to rare species, and could therefore counteract competitive exclusion, thereby maintaining species diversity in communities. A higher proportion of outcrossing plant species tend to be found in less disturbed, biologically complex tropical habitats where pathogens and other natural enemies are more prevalent. Studies support the idea that pathogens maintain genetic diversity by limiting the density or aggregation of individual species. Thus ecological trade-offs among resistance and other life history or physiological traits may restrict the dominance of species in communities, just as the costs of resistance can reduce dominance of resistant genotypes and promote polymorphism, at the community level preventing one or a few species from dominating. But little is known about the role of pathogen diversity and the importance of pathogen host specicity at the community or ecosystem level. By way of their effect on diversity Clay et al. conclude plant pathogens may have an indirect but important role in the functioning of terrestrial ecosystems. Levels of exposure to certain pathogens are considered to have affected the evolution of humans, selecting for genes that confer resistance. Malaria has been a major determinant in the evolution of several human genes, especially those

38

Africa Background to Exuberance

involved in the constitution of red blood cells. It has been suggested malaria was, and is, one of the most powerful forces of selection acting on humans, shaping evolution of several human genes. Pathogens form an ecologically heterogeneous landscape in which spatially separate human populations have been submitted to different selected regimes, leading populations to adapt to their local parasitic conditions thus affecting human biology by determining different life histories. Today the traces of these different evolutionary histories may be found in the genomes of human populations (Guegan et al. 2007). One of the most important corollaries of annual Palaearctic bird migrations is the transport of disease-carrying ticks from one region to the other, such as those infected with Crimean-Congo Haemorrhagic Fever virus (CCHF). From 1959 to 1961, 3.3% of migrant birds examined in Egypt carried ticks, and 8.3% in 1962. Immature tick species recovered were Hyalomma marginatum marginatum, Haemaphysalis punctata, Ixodes ricinus, and a few other species. The most heavily infested by H. m. marginatum were the European quail Coturnix coturnix, European golden oriole Oriolus oriolus, whinchat Saxicola rubetra, European wheatear Oenanthe oenanthe, rock thrush Monticola saxatilis, common redstart Phoenicurus phoenicurus, thrush nightingale Luscinia luscinia, nightingale L. megarhynchus, willow warbler Phylloscopus trochilus, spotted ycatcher Muscicapa striata, tawny pipit Anthus campestris, tree pipit A. trivialis, and red-backed shrike Lanius collurio. Many other birds picked up ticks on their way through Egypt and on the island of Cyprus. The tick Amblyomma hebraeum, of considerable medical and veterinary importance in Zimbabwe, Mozambique, Botswana, and South Africa, has been found on a cow in Bulgaria; while adult A. variegatum have been found on a dog in France and on cattle in Italy. A. lepidum, economically important in East Africa, has been found on the stone curlew Burhinus oedicnemus in Azerbaijan and a white stork at Kharga Oasis, Egypt. The economically important A. gemma of East Africa has been found on cattle in the Crimea and in Israel (Hoogstraal 1979). These examples show how climate patterns, disease, and faunal behaviour in Africa, are inextricably linked with the same factors in Europe, in spite of the Sahara desert.

1.15

Population Limitation

Howard and Fiske (1911) referring to specic species of moth in the United States, asserted that diseases did not as a rule become effective as a population controlling factor until the insect had increased to far beyond its average abundance. Bodenheimer (1958) added that in almost all cases where diseases were believed to be the driving factor limiting outbreaks, closer inspection revealed this was not so. Although lemming Lemmus lemmus irruptions often succumb to a bacterial epizootic the lemmings would have died anyway. The epizootic was caused and advanced by unfavourable climatic conditions. Epizootics may be one of the density-dependent factors which eventually help to reduce numbers in

1.15

Population Limitation

39

a population outbreak, but in their absence they are easily replaced by other densitydependent factors2. Although we may say that weather controls the equilibrium level of the population in conjunction with the density-dependent structure, the existence of an equilibrium density depends not only on the density-dependent structure of the population but also on the total effect of the density-independent factors involved, among which some climatic factors could be major. In the case of Serengeti wildebeest, although in the presence of rinderpest the population was suppressed, under periodic unfavourable climatic conditions food became a limiting factor. With elimination of rinderpest a much higher population level was reached before food became a limiting factor because the latter was caused by an excessively dry season which was density independent. In other words, there was no food whether it was for one wildebeest or ten. Uvarov in 1931 disputed the theory that all living organisms were in a stable equilibrium as far as their relative numbers were concerned, asserting climate ultimately affected numbers; but climate does not regulate numbers. Some animal populations persist at a comparatively steady level in numbers for a long period of time, while others uctuate between extremes. Some fail to maintain themselves, particularly in new habitats, and others establish themselves rmly. These variations provide a central issue of the study of animal populations, posing the question why do animal populations behave as they do? (Royama 1992). Dionysius, bishop of Alexandria about A.D. 255, was perhaps the rst to write about population, bemoaning its decrease through disease,
. . .men wonder, and are at a loss to know, whence come the constant plagues; whence these malignant diseases; whence those variegated infections: whence all that various and immense destruction of human lives. Wherefore it is, that this mighty city [Alexandria] no longer cherishes within it such a number of inhabitants, from speechless children to the aged and decrepit, as it formerly had of those whom it could pronounce rm and vigorous in years. But those of 40 years and up to 70, were so much the more numerous then, that their number cannot now be made up.... And those who in appearance are but the youngest, are now as of an age with those formerly the oldest. And yet, though they constantly see the human race diminishing, and constantly wasting away, in the very midst of this increasing destruction, and this annihilation, they are not alarmed. (Cruse 2006)

But Leonardo da Vinci about 1509 appears rst to have speculated upon population increase and on evolution, indicating predation and disease as foremost causes of population control,
Nature, being inconstant and taking pleasure in creating and making constantly new lives and forms, because she knows that her terrestrial materials become thereby augmented, is more ready and more swift in her creating, than time in his destruction; and so she has ordained that many animals shall be food for others. Nay, this not satisfying her desire, to the same end she frequently sends forth certain poisonous and pestilential vapours upon the vast increase and congregation of animals; and most of all upon men, who increase vastly because other animals do not feed upon them. . . (Richter 1883)

More in his Utopia (1516) mentioned great pestilent plagues as an exceptional cause of depopulation, want placing the main restriction on increase, and

40

Africa Background to Exuberance

Machiavelli in his Discorsi (1531) remarked that an excessive population would be diminished by want and diseases. Considerably later, in 1588, referring to urban concentrations Botero advanced the idea that human populations are restrained at higher densities by the carrying capacity of the environment, an idea elaborated upon two centuries later by Malthus following upon several authors subsequent to Botero. Botero concluded mankind was potentially as fertile in his day as in ancient times but populations did not grow any longer because the resources of the environment were insufcient to support larger populations. Population growth was halted by famine, contagious diseases encouraged by overcrowding, and sometimes by wars, earthquakes, oods, and other accidents, but generally, the fruits of the earth do not sufce to feed a greater number. . . And if it [a city] do not increase in innite I must needs say it proceedeth of the defect of nutriment and sustenance sufcient for it. Botero thus concluded the capacity of the environment to support population was nite and diseases and epidemics were secondary to means of subsistence to limitation. Cole (1957) considered little had been added in terms of the broad concepts of population regulation since Boteros day. Hale in his Primitive Origination of Mankind (1677) anticipated Malthuss theory of geometric population increase by more than a century, So that in the compass of about 34 Years the number of two, namely the Father and Mother, is increased to the number of eight. . . so that in 34 Years they become increased in a quadruple proportion. . . by a Geometrical Proportion their Increase is multiplied proportionable to the Excess of their number above Two. And Malthus (1798) only copied him when he wrote that in warmer and more populous towns an insufciency of food led to epidemics either in the shape of great and ravaging plagues or less violent though more constant sicknesses. Extracting from Short (Short 1749), who produced a table of all the plagues, pestilences, and famines which he could nd, Malthus calculated that plagues or other great epidemics had occurred since A.D. 1 every four-and-a-half years in countries which were better known, and famines about every seven-anda-half years. Perhaps inuenced by Walter Charleton (d1707), although making no reference to him3, Derham in 1713 asserted the various species of animals differ in their organs and ways of life because . . . the surface of the Terraqueous Globe is covered with different Soils, with Hills and Vales, with Seas, Rivers, Lakes, and Ponds, with divers Trees and Plants, in the several Places, and that the various species of animals are manifestly adapted for the places in which they live and for the ways in which they live, continuing, The whole Surface of our Globe can afford Room and Support only to such a Number of all Sorts of Creatures; and if by their doubling, trebling, or any other multiplication of their Kind, they must starve, or devour one another. This is prevented by Balancing the Number of Individuals (his italics) of each Species of Creatures, in that Place appointed thereto, the balance of numbers being kept even because the length of life in each species is adjusted to its ability to increase. Voracious beasts and birds have long lives but their rate of increase is small so that they do not overstock the world. Insects exemplify animals with great reproductive ability but short lives. Human longevity, he believed, was adjusted to the available space.

1.16

Stability or Chaos?

41

Whereas Derham explained everything in terms of Divine Providence, the orie du fundamentals of comparative demography were there. Brckner in his The u `me Animal (1767) stated in the animal world, as in the plant world, species Syste could not exist other than in a certain proportion with the area of land which they occupy, for as soon as the numbers of individuals exceed this proportion, they decline and perish because everywhere where there is a superabundance of life there is a food famine. Adam Smith in his Wealth of Nations (1776) noted, Every species of animals naturally multiplies in proportion to the means of their subsistence, and no species can ever multiply beyond it. Ortes in his Riessioni sulla Popolazione delle Nazioni per rapporto allEconomica Nazionale (1790) stated the check to the increase of animals was lack of food and recognized, as had others, human populations tended to increase in a geometric ratio. When Malthus published his Essay on the Principle of Population he was saying nothing that had not been said before. Practically all writers who discussed the subject and whose works appeared in the two decades before the publication of Malthuss Essay, accepted that populations depended upon food supply (Stangeland 1904). Buffon (1929) wrote that an unbounded fertility of every species was counterbalanced by the innumerable causes of destruction which were perpetually reducing the produce of that fecundity so as to preserve nearly the same number of individuals in each species. But this was not a xed number, so populations oscillated in size between limits. An excess of fecundity in one year was followed by relative sterility the next, noting for example that some insects with several generations per year were capable of multiplying more than their food plants which had only one generation each year. He disagreed with Aristotle that heavy rains caused the decline of populations of eld mice, but contagion was a necessary consequence of too great a mass of living matter assembled in one place. The prodigious increase of eld mice was checked only by their cruelties to each other when provisions became scarce. However he placed predation rst among controlling factors, noting that rabbits would reduce the country to a desert if it were not for dogs and ferrets.

1.16

Stability or Chaos?

Elton (1930) remarked . . . the balance of nature does not exist and perhaps never has existed. Community structure of ecosystems is controlled by biotic interactions where abiotic variability is small, the classical equilibrium condition. But these same abiotic variables come to control communities when climate is highly variable, resulting in a non-equilibrium condition (Wiens 1984). Non-equilibrium systems are characterized by high levels of variability in time and space of biomass production, and what were formerly thought to be fragile semi-arid systems prone to destruction through overgrazing are now considered unlikely. Production potentials of both grassland and herbivores are kept low through the impact of drought or other episodic events such as disease (Scoones 1995). Whereas the theory has been

42

Africa Background to Exuberance

developed in respect to stock raising, the principles apply equally whether relating to cattle or to Kalahari wildebeest. In non-equilibrium dynamics an animal population never reaches a level where density dependent factors operate, the population being limited largely by density independent factors, such as rainfall, and thus may be the dominant form of dynamics in arid areas. The concept of carrying capacity, in broad terms the number of animals that a range can support without deteriorating or the balance of grazing pressure against the regenerative power of the plants, was Clementss (1916) theory of succession applied to grassland. Grazing pushed the successional sequence back to some form of sub-climax. In wild life biology carrying capacity is dened as K, the ecological carrying capacity, the asymptotic level of a logistic curve of growth in numbers at which point there is no surplus primary or secondary production, the increasing number of herbivores checked by the availability of forage, the rate of production equalling rate of consumption. This consumption is not simply by ungulates, a great proportion of primary production is consumed by invertebrates but this is seldom measured. At K livestock may be plentiful but will not be in particularly good condition, neither will vegetation be as dense or the plant communities necessarily composed of the same species as would be the case at a lower level of consumption. As the animal population grows beyond a point halfway to two-thirds of the asymptote increasingly high rates of mortality and falling birthrates cause the rate of increase to fall ultimately approaching zero. For managers of livestock, carrying capacity is this point halfway to two-thirds of the asymptote, the economic carrying capacity. Thus carrying capacity means differ according to the objectives. Among pastoral nomads it is K, for to them numbers of animals are more important than quality because in a severe drought there is a greater chance of one in ten lean animals, say, surviving, than one formerly fat animal. Many different Orders of mammals, and some birds, uctuate in a periodic manner, but we are no closer today to really knowing the cause than Elton was. The best known examples are those of the colder climates of populations of lemmings in Norway and varying hares Lepus americanus in Canada. These build up to a maximum, cycles which take 3.6 years in the lemming and 10 years in the varying hare, and then almost the entire populations succumb to fatal diseases, other than those lemmings which commit suicide by entering water. In the tropics and subtropics there appears to be more of a balance. In Serengeti wildebeest populations it has been shown disease may act in a depressant manner upon the population but not in a periodic manner (the yearling disease appears to have had a constant effect), and in the absence of other factors, disease or human hunting, the population is controlled by the food resource, population reduction taking place in poor seasons even although the population number may be below its potential of good years. Elton (1925) pointed out that in the Tropics temperature varied by as much as 0.6 C between the period of sunspot maxima and minima, the effect diminishing to the north and south, which could have a signicant effect upon tropical ecosystems as it shifts the isotherm by over 130 km, but although the periodic temperature change related to sunspot activity ought to reveal a greater effect in the tropics than it does in northern climes where the temperature effect is

1.16

Stability or Chaos?

43

weak, periodicity is not apparent; however extensive work on rodents over long time periods has yet to be conducted. Prior to chaos theory, dened as bounded uctuations with sensitive dependence on initial conditions or an apparently random behaviour of a system over time, in fact the result of very predictable rules chaos and statistical periodicity not being mutually exclusive concepts (Turchin 2003), there was a school of thought that complex ecosystems were more stable than simple ones. It would seem to make good intuitive sense that a system with many links is more stable than one with few links or feedback loops. Thus if a herbivore species is attacked by several predator species, the loss of any one of the predator species is less likely to allow the herbivore to erupt in numbers than if only one predator species were present and that single predator species disappeared. But there is no convincing evidence diverse natural communities are in general more stable than simple ones. Thus uctuations in lemmings in Arctic ecosystems are no less violent than those of say, formerly, South African springbok in the complex sub-tropical ecosystem. Very high species diversity is frequently associated with areas which have relatively constant physical environmental conditions over the course of a year and a series of years, and because of a high degree of specialization the species have a low ability to recover from major interventions. Goodman (1975) questioned the diversity-stability theory that more diverse communities will be more stable than those less diverse. While querying what was meant by diversity and stability he considered the apparent stability of tropical biota may well be an illusion, for even considerable uctuations might go undetected in such complex assemblages as the rainforest has to offer. He concluded there was no simple direct relationship in ecosystems and the belief that more diverse communities are more stable is without support. Early twentieth century ecological theory leaned towards evolutionary processes tending to produce organisms and assemblages of progressively greater self-regulating capabilities, as in the theory of plant succession and its tendency towards community stabilization, ideas founded in the popular teleological philosophies of nature as promoted by Spencer in 1866, the underlying thought being that variety must have some purpose, as Leonardo da Vinci had speculated at the beginning of the sixteenth century. Bond and van Wilgen (1996) stress the dynamics of African savannah systems are notoriously complex, inuenced by combinations of drought, herbivores, humans, elephants, re, insect outbreaks, competition, and soil conditions, and to this we could add parasites and pathogens, all interacting in complex and unpredictable ways. They note that it seems remarkable such an unstable mix of grass and trees should exist in apparent dynamic equilibrium over such large regions. The Eastern and Southern African savannahs harbour the greatest diversity of large mammals found in Africa, and in the world, and their oral diversity is also high with an average areal richness of 1,750 and 50 species, compared with rain forest of about 2,020. The richest zone, the Somali-Masai region, contains some 2,500 plant species, of which 50% are endemic. Primary and secondary productivity of the semiarid and arid rangelands is thought to be constrained more by density-independent

44

Africa Background to Exuberance

factors, such as climatic variability, than density-dependent factors such as stocking rates and grazing pressure. In other words non-equilibrium dynamics, the theory of a climax vegetation with a carrying capacity being generally discarded. Nonequilibrium dynamics holds that a oristic structure is a consequence solely of opportunities for immigration and accidents of extinction, and that there are no processes which favour predictability or uniformity of species composition in forest succession following disturbance. In recent years concepts of range management in relation to cattle stocking which were developed at the beginning of the twentieth century and came to dominate theory surrounding savannahs in Africa have been questioned, theories of carrying capacity and ecological sustainability being rejected in favour of non-equilibrium dynamics. These criticisms would apply equally to hippopotamus and wildebeest as much as they may to stock rearing. Some see species richness as playing a role in enhancing the productivity, robustness, and resilience, of ecosystems, and it may also buffer the impact of vector-borne diseases (Kinzag et al. 2002), and indeed contagious diseases also. Others consider increased diversity conferring increased fragility upon a system and increase in diversity or complexity resulting in increased community stability may happen sometimes, but there is no necessary connection. The more complex or diverse a system is, then the less likely it is to retain all of its species in the long term. In the tropical forest the climax is dominated by one or a few of the most successful species so diversity is low. But there is little or no evidence of real ecosystems ever being in equilibrium and it is the continued instability of systems which allows for the continual coexistence of multiple species (Walker 1989). Balanced systems where environmental disturbances and other random events can play a signicant role may be relatively rare. Most natural ecosystems can be perceived as recovering from some form of disturbance, whether climatic, animal, or anthropogenic, a concept now known as non-equilibrium ecology whereby competitive interactions between species are relaxed, and coexistence can occur even if species have the same patterns of resource use. Swaine (1989) points out that catastrophes such as re, windthrow, or drought, need occur once only in a century or less to exert a permanent inuence on forest composition. Recent studies of African savannah ecosystems have shown them to be inherently unstable in their ecological diversity, greatly inuenced at different times and to different degrees by uctuations in climate and the impact of man, re, and herbivores (Lamprey and Waller 1990). Looked at in another way, they are rarely in equilibrium, normally functioning ecosystems experiencing a range of conditions, change being the normal condition. Movement between the range is essential to maintaining the proper functioning of the ecosystem, giving it resilience (Holling 1973). Walker used Botswanas Savuti marsh as an example of instability in the savannah, an area spatially very diverse with animals using different parts at different times, those areas far from dry season water providing emergency forage in drought years the density of ungulates being far below that which the vegetation could support in an average year. The system is open with a considerable movement in and out of migratory herbivores, 16,500 zebra, 2,500 buffalo, 1,500 tsessebee Damaliscus lunatus and 600 wildebeest. The zebra and buffalo are there during the

1.17

Do Population Cycles Exist?

45

rains, tsessebee during the dry season, and wildebeest presence is more variable. Elephant numbers can be high also, their density depending upon surface water. The strength of the biological interactions is variable and weak, as one or more species moves in or out of the area conditions are never constant for long enough that strong biological interactions develop. The system is driven by external episodic events, in particular the supply of surface water in the Savuti Channel, drought, re, and disease. The size structure of the acacia woodlands, all mature even-aged trees dying as a result of senescence and elephant damage, indicated the woodlands are unstable, declining with an absence of regeneration due to high browsing pressure. Walker considered the trees became established at the turn of the twentieth century when the Savuti Channel dried up (due to tectonic events) and rinderpest destroyed many of the ungulates, while elephant numbers were low due to excessive hunting (Spinage 1990); claiming the combination of these events reduced browsing pressure long enough to allow the extensive stands of Acacia spp. to develop. But zebra are unaffected by rinderpest and any reduction of other herbivores would have contributed to the grass cover being undergrazed and therefore ercer res due to more fuel retarding tree seedling growth. The principle pressure relaxed would have been elephant browsing, as has been found to be the case elsewhere, the same pressure preventing regeneration in the 1980s. Disturbances to ecosystems should mean that resources are rarely close to exhaustion and thus competition for them should not be so important. However a balanced ecosystem implies that although disturbances may occur there is a quick return to the status quo, thus non-equilibrium ecology may simply be seen as the uctuations around an equilibrium.

1.17

Do Population Cycles Exist?

The African tropics and subtropics have witnessed spectacular population increases of mammals ranging from elephants downwards in size, although that of elephants is clearly man induced related to ivory exploitation, but there is no rm evidence of cyclic periodicity in the increases of other animals. Rather, populations relate to food supply which in turn is dependent upon climate. Even if cycles were intrinsic these could only operate if climate provided food enough for the increase phase. Whether climatic uctuations relate to sunspot cycles is a moot point, but if so, and these cycles feed through to animal populations, they are muted in effect. Forest invertebrates, especially butteries, swarm seasonally in incredible numbers, but again we have no time-related studies. However few known species in the world exhibit obvious cyclic uctuations, notably among the few being the varying hare and its synchronous 811 year population cycles across the boreal forests of North America. Theory indicates that such population cycles are produced by time delays in density dependent factors affecting reproduction or survival. When density is high the hares show decreased natality, increased starvation, and increased predation, producing time delays in population regulation. Food supply and predation are considered the main factors causing the cycles, although other factors such as

46

Africa Background to Exuberance

extrinsic effects of weather and plant secondary compounds have been implicated. However recent experimental work with varying hares demonstrates it is the physiological mechanisms which underlie individual and population level responses of prey to predator-related stress, causing increases in maternal stress through glucorticoid production. Predator induced elevated levels of glucorticoid concentrations through the hypothalamic-pituitary-adrenal axis, which initially stimulate the ight response, caused a decline in reproductive output both in number and tness of offspring. As hare populations increase so do their predators but with a lag of 12 years, when their numbers begin to initiate a decline in the prey directly causing up to 83% of deaths. This is combined with a deterioration in reproduction brought on by stress. Although elevated maternal glucorticoid levels may cause a decline in reproductive output they may ultimately increase tness by promoting juvenile survival through transmitting the fear response to the offspring, making them more fearful and thus more predator aware (Sheriff et al. 2009). To what extent heightened glucorticoid levels might affect the reproductive status of males was not measured. Although the effect in females serves to explain the cyclic nature of varying hare numbers it does not explain the spatial synchronicity. Glucorticoid concentrations can be affected also by density and social status, weather, and parasitism, and theoretical models suggest macroparasites can cause oscillations in population abundance. Apparently benign endoparasites may have strong effects on host dynamics if they act synergistically with other mortality factors, with no direct effect on demography they may affect host dynamics indirectly by interacting with other species in the system (Ives and Murray 1997). But certain parasites can cause juveniles to delay maturation until the next reproductive season, and reduced fecundity following recovery from disease can affect a populations dynamics also. Modelling interactions of eld vole Microtus agrestis cowpox Vaccinia infection indicates disease could cause multi-year cycles if its effects on fecundity are sufciently strong (Smith et al. 2008). Pedersen and Grieves (2008), studying American white-footed mice Peromyscus leucopus and deer mice P. maniculatus, considered that intestinal parasites may exert a signicant effect on host health and population level consequences, and demonstrate that multiple factors may often be driving long-term small mammal oscillations. In a strictly mathematical and statistical sense, in which the term has from time to time been used, a cycle can be dened as any oscillation that has a statistically signicant periodicity, this therefore can be as short as 2 years, but ecologists usually reserve the term for an oscillation taking three or more years to repeat itself, as the former is regulated by intrapopulation processes such as competition for food and space, the latter by interpopulation processes such as food or predators (Berryman 2002). Many suggestions have been advanced to explain synchrony in cycles, Canadian lynx Lynx canadensis cycles, for example, exhibit remarkably regular 10 year cycles which are also very well synchronized across all regions of Canada. Lockyer in 1874 very appropriately wrote, Surely in meteorology, as in astronomy, the thing to hunt down is a cycle, and if that is not to be found in the temperate zone, then go to the frigid zones or to the torrid zone, to look for it. . ..

1.17

Do Population Cycles Exist?

47

Meteorological factors, sunspot cycles, ozone cycles, ultra-violet ray cycles, forest re cycles, and lunar cycles, have all been proposed, but without convincing evidence; and some, such as the ozone and ultra-violet ray cycles, have been rejected long ago. Cole (1957) concluded regularity of population cycles seemed no greater than that encountered in a sequence of random numbers. The tacit assumption is that the cause of the population cycles, or the occurrence of outbreaks, is also the cause of the synchrony, i.e. there is one common extrinsic factor which governs the cyclic uctuations in the populations and hence the synchrony among them. A more likely possibility is that if two regional populations have the same density-dependent structure, then they will be correlated under the inuences of density-independent factors such as climate if the factors are correlated between the two regions. This, the Moran theorem, implies that the cause of the synchrony can be completely independent of the cause of the cyclic population uctuation. The Moran theorem is generally and universally applicable because it does not depend upon any particular assumption about the pattern of weather sequence. There just needs to be an extrinsic density-independent factor inuencing reproduction or survival and correlated across regions (Royama 1992). Asking the questions why do population outbreaks in particular species happen more or less regularly in certain locations, but only irregularly or never in others, and why do some organisms become extremely abundant one year and then seem to disappear a few years later? Turchin (2003) has described how, beginning with the pioneering work of Elton (1924) on uctuations of antarctic species which purported to show periodic uctuations in certain animals must be due to climatic variations, becoming a central issue in ecology with publication of his work Voles, Mice and Lemmings in 19424 workers have tried to identify the driver behind these quasi-regular oscillations, arguing between food and predation following Lotka (1925), who by the use of mathematical models suggested population cycles were generated by endogenous causes. The extensive fur records from Hudsons Bay and other regions in an unbroken series dating from 1752 were given rst by Poland (1892) but he made no comment on uctuations, Hewitt (1921) being rst to analyse them. Hewitt concluded the animals could be divided into three main groups: rstly, herbivorous rodents such as mice and rabbits which increased in numbers until overcrowded, when epizootic disease almost wiped them out, their numbers decreasing rapidly to a minimum. Secondly, predatory animals which depended directly or indirectly upon the former for their subsistence. These showed a fairly regular periodic uctuation in numbers, abundance being correlated with the abundance of animals on which they fed, although the sher (sable) Martes pennanti may have a distinct periodic uctuation which does not appear directly related to uctuations in the numbers of any particular prey animal. Thirdly were the omnivorous animals which did not show any marked periodic uctuations. Lotka concentrated on predation, the models dening these cycles, particularly those of rodents, rarely including parasites and diseases. Although taking account of micro or pathogenic parasites, i.e. diseases, and dividing the hosts into susceptible, infectious, recovered and sometimes, exposed, Turchin showed the Lotka-Volterra equation of predation is similar to a disease epizootic, susceptibles becoming prey

48

Africa Background to Exuberance

and infectives predators. Thus epizootic models belong to the general class that contains predatorprey, parasitoid-host, and herbivore-plant, models, In short, they are all trophic models, and all are prone to oscillatory dynamics. There are important differences, such as the heterogeneity between hosts of their likelihood to become infected which is widely present in natural populations. Turchin concluded the overwhelming majority of examples of population oscillations in nature is explained by the mechanism of specialist predation, with a few additional cases involving other kinds of trophic interaction (food and parasites). But there are no complex dynamics driven by intrinsic mechanisms, interspecic competition, mutualisms, commensalisms, etc. The great Norwegian lemming outbreaks with their spectacular long-distance migrations exhibit a persistent long term pattern with major irruptions occurring at roughly 30-year intervals in 1755, 1787, 1810, 1840, 1872, 19021903, 1938, and 1970. Following the 1970 migration local peaks were observed in many areas in Lapland in synchrony with vole peaks in 1974, 1978, and 1982. No periodic climatic factor of sufcient strength, large enough amplitude and appropriate period, has been documented for rodent outbreaks, and the variation in sunspot activity is much longer than 5 years. However on average the sunspot cycle is about 1.6 years longer than the lynx cycle, 11.2 compared with 9.6 years, so that two such cycles starting in phase will gradually drift apart and when in phase in one area will be out of phase in others. No evidence for parasite-driven rodent cycles has emerged. Because of their complicated life cycles, a 35 year rodent cycle is too short for macroparasites to track it, but they can track the 10 year varying hare cycle (Hanski and Henttonen 2002). Berryman (2002) concluded that endogenous population cycles can be caused by food web dynamics, strong feedback between consumers and their resources can generate cyclic dynamics in both populations. Chitty (1996) considered all species were capable of limiting their own population density without either destroying the food resources to which they are adapted, or depending upon enemies or climatic accidents to prevent them from doing so. The abundance of large-herbivore populations is widely held to be limited by extrinsic factors, most commonly food supply, predation, or both, although we know in the case of Serengeti wildebeest disease in the form of rinderpest was limiting until this factor was removed. But factors which limit the size of large herbivore populations may or may not also regulate them, depending upon whether or not they operate in a density-dependent fashion (being a contagious disease the extent of rinderpest infection is determined by population density). But the ultimate driving factor, whatever the proximate cause, in temperate to tropical latitudes as Elton originally supposed must be climate which determines food supply. Even in the boreal climate a relatively small rise in summer temperature may be the driving cause reected in greater abundance of food. Limitation is the process which sets the equilibrium point, the numbers at which a population stabilizes. Regulation is the process whereby a population returns to its equilibrium after increasing or decreasing. The arguments surrounding these processes, which are often confused, are distinct from the phenomenon of regular periodic oscillations in population numbers. Sinclair (1989) concluded the majority

1.17

Do Population Cycles Exist?

49

of large terrestrial mammals, including all ungulates, was regulated by density dependent mortality related to food shortage. While predation could be an important limiting factor in large herbivore populations there was in general no empirical evidence that it could be a regulating factor. Bayliss and Choquenot (2003) concluded that if predation does not commonly regulate the abundance of largeherbivore populations then this must be by intrinsic (socially mediated) mechanisms, debilitating effects of disease or parasites, or food availability. But it has been argued that in highly variable environments, factors such as unpredictable rainfall could introduce signicant degrees of density-independent variation in food availability and herbivore abundance, which when combined with lags and overcompensation in vegetation and herbivore responses can obscure any tendency that density may have been towards equilibrium. Sinclair and Krebs (2003) state that food supply is the primary factor determining population growth rate in animal populations but this can be modied by predators, social intra-species interactions, and chance disturbances. While any process that affects population density will be a limiting factor, only density-dependent factors are also regulating factors (Sinclair 1989). Large herbivores face four effects: seasonal environmental variation throughout the year; climatic uctuations which can alter the impact of this variation; densitydependent responses when populations overshoot a threshold density; and changes in abundance or behaviour of predators or diseases. Density-independent limitation and density-dependent regulation co-occur in most populations so that the impact of density-independent factors such as weather typically increases with population density. Received wisdom is that infant mortality somehow implies an unhealthy population, but in nature the opposite is true. Impaired infant survival means there is no more room in the population for new recruits. Population control operates on the principle of dead mens shoes, the new generation can be accommodated only in places vacated by the old. Studies of temperate zone mammals have revealed often that under harsh winter conditions fetal reabsorption might take place, and it was thought such a mechanism might control population increase. Studies of large African mammals rarely reveal deciencies in the female, there is almost always 100% breeding success except for the very old and the odd female with pathological disturbances or otherwise anomalous animals. The female is rarely, if ever, sacriced for the offspring. If a female dies in dystocia, as has been observed, the neonate dies also. If conditions become very unfavourable in the period leading up to parturition the fetus does not parasitize the females last reserves, it is born in a hypoglycaemic state and fails to survive. The female is thus not under lactation pressure and may survive to succeed next season. But it is likely that sufcient reserves will be mustered to produce a viable offspring. If predation is a controlling factor then it is at this stage that it operates, not on the adults. If the population is at carrying capacity and further young fail to be recruited into the population, should conditions become more favourable the population can respond instantly with recruitment. If mechanisms operated to prevent the female conceiving then the chance of taking advantage of improved conditions would be

50

Africa Background to Exuberance

lost. Thus successful reproduction followed by early death of the newborn is the most effective manner of limiting a population and of ensuring its continuity. Diseases add complexity to the parameters. Thus to take as an example human populations in pre-colonial Africa when drought could result in sharp population declines due to mortality from starvation, as the drought progressed and weakness spread through a population latent smallpox infections frequently erupted into fatal epidemic proportions. Plotted against time population decline would be found correlated rstly with decline in rainfall reected in food supply, and secondly with disease. Disease might be a signicant factor in microtine rodent declines because they harbour pox viruses but the models do not take this added complexity into account, although Turchin does refer to the work of Ives and Murray (1997) who postulate that another ecological mechanism, parasitism, may affect the workings of the primary one, predation, in driving varying hare population cycles. Royama (1992) concluded it was reasonable to consider the varying hare cycle was essentially a predatorprey cycle and the hare-vegetation interaction contributed to the remarkable stability of the 10-year cycle, with cycle synchrony across regions maintained by the Moran effect. In general there are no long term records for evidence of cyclic population phenomena from Africa, although Stevenson-Hamilton (1947) alleged the occurrence of uctuations dating from 1902,
In any game country where man has not yet interfered with the intricate relations between wild creatures, the carnivorous animals are exactly proportioned to the stock of animals forming their food. So well is the balance adjusted, that a temporary increase or decrease in one direction is followed by a corresponding change in the other . . . The life history of every species in a wild state proceeds not in a straight line, but in a series of curves, which are mainly inuenced by the incidence of the available food supply, which as it is temporarily abundant or otherwise, affects benecially or detrimentally the general health of the animals, and so renders them more or less resistive to the attacks of epizootes, with which. . . nearly all are in greater or less degree affected.

He claimed despite the presence of abundant hunting dogs there was a constant rise in the reedbuck Redunca arundinum population of the Sabi GR between 1902 and 1917, then declining suddenly so that by 1920 it seemed almost extinct south of the Olifants River. Recovery was extremely slow, reedbuck still being very rare 20 years later while hunting dogs had declined to vanishing point. He attributed the reedbuck decline to intensive grass burning removing their preferred cover. Steinbuck Raphicerus campestris had much the same history from 1914, becoming rare after 1920 but increasing from 1930, more than recovering their former abundance by 1940. But following 10 years of drought which began at the end of 1925 there was a progressive decrease among sable antelope, and after1932 blue wildebeest, although most of the latter emigrated. Waterbuck and warthog became greatly reduced in numbers, but browsers such as kudu Tragelaphus strepsiceros, and especially impala, increased and spread, favoured not only by an absence of hunting dogs but an increase of acacia and other shrubs due to fewer grass res during the drought. Zebra suffered less and increased after 1935. Hunting dogs were numerous south of the Sabi River in 1902 and remained so to about 1927 despite

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Do Population Cycles Exist?

51

rigorous control, discontinued in 1931, but decline ensued until by 1933 they had nearly disappeared, remaining rare in numbers to 1940 and beyond. Indicative perhaps of canine distemper virus CDV the side-striped jackal Canis adustus population behaved likewise, beginning to decrease sometime between 1920 and 1930, disappearing from most of its former range by 1940 its place taken by the black-backed jackal C. mesomelas. The latter then declined also. These decreases were mirrored by the spotted hyaena Crocuta crocuta population, which began to increase again from about 1933, soon approaching its former numbers. StevensonHamilton wrote,
All the smaller creatures, preyers and preyed upon, are, equally with the larger, subject, under natural conditions, to the law of alternate curves of specic elevation and depression. Besides the major peaks and alarming depressions which occur among individual species from time to time, there are annual curves of alternating abundance and want, which affect herbivora and carnivora conversely.

But when game density is low in good seasons because it is dispersed, then lion numbers are low because the lions nd prey harder to obtain until it has increased to a point which makes it more accessible. Lion numbers then increase again. Ogutu and Owen-Smith (2005) analysed Kruger NP records of large mammals from 1965 to 1996 and concluded 12 species of ungulate populations: zebra, warthog, giraffe Giraffa camelopardalis, buffalo, greater kudu, eland Taurotragus oryx, waterbuck, impala, tsessebe, wildebeest, roan antelope Hippotragus equinus, and sable antelope H. niger, displayed cyclic variability in numbers with half cycles ranging between 10 and 18 years, associated with lagged rainfall between 3 and 10 years previously for different species, the rainfall cycle being approximately 18 years. Species responded in contrasting ways to rainfall: zebra, giraffe, eland, impala, wildebeest, and sable antelope reaching highest abundance during periods of low rainfall; warthog, buffalo, greater kudu, waterbuck, tsessebe, and roan antelope, under high rainfall. This was inconsistent with the expected response if the oscillations were driven by the inuence of rainfall on food availability, seeming instead to be the outcome of predatorprey interactions affecting the relative susceptibility of different species, i.e., the habitat being open or closed, exposing or concealing predators. Ogutu and Owen-Smith concluded predatorprey oscillations were manifested even in such multi-species assemblages, with external forcing by rainfall variability helping to synchronize patterns of population variation. Although periodicity may not be apparent, some species undergo uctuations in numbers of striking proportions, most notable being the locust. But in forest and woodland caterpillars are among the highest herbivore consumers although they tend to be specic in choice, and even snails can undergo damaging irruptions. Schlippe (1956) reported in 1950 among the Azande in the south-west Sudan, In April one could observe small patches of the ground covered with innumerable white bodies of the size of a pin head. In May and June the snails grew and spread out, devouring every crop on their way. Here and there people swept them together into heaps and burnt them. . . the early crops-maize, sweet potatoes and groundnutswere destroyed in big patches. . . By July and August the snails had grown bigger

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Africa Background to Exuberance

than peas and had spread over the whole area . . .. Unfortunately the species was not identied. Caterpillars of the moth Elaphrodes lactea feed on Caesalpiniaceae species in miombo woodland and are capable of spectacular tree defoliation over wide areas, although the moths range is limited essentially to south of DR Congos Shaba region and to Zambia. Outbreaks were witnessed in the Lubumbashi region of DR Congo in 1934 and 19691970. It was calculated that at peak density the monthly leaf consumption of the caterpillars was 733 m2/ha, equivalent to 98 kg/ha, and their faecal dry weight was 90 kg/ha. Although concentrating on Brachystegia and Julbernardia species they will turn to other species if necessary. In March 1971 all the Pericopsis angolensis (Baker) van Meeuwen trees in an area of southern DR Congo were defoliated when the Uapaca spp. were attacked by a Parasa sp. caterpillar. The effects of these irruptions are unknown (Malaisse 1978). The mopane caterpillar Gonimbrasia berlina is specic to Colophospermum mopane, defoliating complete trees often over large areas. The leaves regrow within weeks and there is sometimes a second much smaller outbreak in the same season but typically several years elapse between outbreaks. The caterpillars briey accelerate nutrient recycling through their droppings. Another lepidopteran example of irruption is provided by the army worm, the caterpillar of the moth Spodopterus exempta, which has a wide distribution and feeds on a greater variety of plants, irrupting with much greater frequency. Like swarming locusts it undergoes a phase change when irrupting. At low density the larvae are mainly green in colour, solitary, sluggish, and inconspicuous with low feeding rates. At high density they are predominantly black in colour, conspicuous, and gregarious, active voracious feeders, and exhibit marching behaviour and synchronized development. The gregarious phase grows faster than the solitary phase and transition between forms can occur in one generation. If raised under crowded conditions gregarious phase larvae are produced, but if raised singly then solitary phase larvae result. Eggs are laid in masses thus the survival rate of the eggs probably determines which phase results. Adults from gregarious larvae migrate readily whereas those of solitary larvae tend to oviposit in the natal area. During irruptions migration of the adults leads to progressive spatial shifts in the outbreak areas at monthly intervals, the generation time. The appearance of dark coloured forms at high population density has been observed in many other phytophagous Lepidoptera and Orthoptera. The study of periodicity has taken on a renewed lease of life as the science of chronobiology. Life having its origin on a rotating world, some hold that periodic rhythms are central to all forms of life from the diversity of genera on the ocean oor with cycles of millions of years, to circadian rhythms in human blood pressure. Apart from cycles of days, weeks, and months, there are cycles of some 11, 22, 33, 50, 500 and myriadennian years. These are genetically programmed self-sustaining and self-reproducing relating to longstanding environmental cycles in the electromagnetic spectrum in the visible range, photics such as the day and seasons, and the invisible or beyond, nonphotics, which relate to radiation from space weather, broadly galacto-helio-ionosphero-geomagnetics, gravity, UV ux and whatever else can be measured in time in the cosmos (Halberg et al. 2009). Synchronous

1.18

Notes

53

periodicity in populations may thus be a genetically based extension of the circadian rhythm.

1.18

Notes

1. It is considered by some the South American term savannah has unnecessarily crept into African ecology causing considerable confusion, but its use is preferable to using several terms, and it is here used in its general sense of at or rolling grassland plains, which may be open or lightly wooded, as compared to deciduous woodland or forest. Kenneth (1963) dened it as Subtropical or tropical grassland with xerophilous vegetation and scattered trees; transitional zone between grasslands and tropical rainforests. but I include grassland without xerophilous vegetation in the sense of not grassland, and scattered trees, in the denition. Nye and Greenland (1960) consider that by laying emphasis on the herb layer as the ecologically dominant stratum this satisfactorily separates savannah from woodland or forest. 2. Bodenheimers inference that weather determines the reproduction and survival of animals and regulates some populations, particularly insects, has been shown to be false. Weather may govern the pattern of population uctuation but it does not regulate the population (Royama 1992). 3. Although it does not appear in his published writings we know Charleton speculated upon adaptations for he explained to Samuel Pepys at dinner in 1,666 that Nature fashioned every creatures teeth according to the food she intended them and he could tell the food of an animal from its teeth (Smith 1906). 4. A number of observers commented upon these uctuations prior to Eltons work: Macfarlane (1905) Mammals of the Northwest Territories, Seton (1909, 1911) Life Histories of Northern Mammals and The Arctic Prairies respectively, and Cabot (1912) In Northern Labrador.