Advertisement

Suffrutex Dominated Ecosystems in Angola

Open Access
Chapter

Abstract

A small-scale mosaic of miombo woodlands and open, seasonally inundated grasslands is a typical aspect of the Zambezian phytochorion that extends into the eastern and central parts of Angola. The grasslands are home to so-called ‘underground trees’ or geoxylic suffrutices, a life form with massive underground wooden structures. Some (but not all) of the geoxylic suffrutices occur also in open woodland types. These iconic dwarf shrubs evolved in many plant families under similar environmental pressures, converting the Zambezian phytochorion into a unique evolutionary laboratory. In this chapter we assemble the current knowledge on distribution, diversity, ecology and evolutionary history of geoxylic suffrutices and suffrutex-grasslands in Angola and highlight their conservation values and challenges.

Keywords

Endemism Geoxyles Miombo Phytochorion Underground forests Vegetation 

Introduction

Open grassy vegetation is a common aspect of Angolan landscapes and is a characteristic part of the Zambezian phytochorion. Grasses are the most conspicuous element of these landscapes towards the end of the rainy season, whereas at the onset of the rainy season many woody species of so called geoxylic suffrutices or ‘underground trees’ (Davy 1922; White 1976) dominate the aspect of the vegetation. Thus, in vast areas of central and eastern Angola, the open ‘grasslands’ are de-facto co-dominated by grasses and geoxylic suffrutices. Closely intertwined with miombo woodlands and with wetlands, suffrutex-grasslands constitute one of the main and most particular ecosystem types of Angola. According to Mayaux et al. (2004), they cover at least 70,080 km2 or 5.6% of the Angolan territory (not including the small scale woodland suffrutex-grassland mosaics of the central Angolan plateau).

The geoxylic suffrutex life form is marked by proportionally massive underground woody organs, in literature often termed as lignotuber, xylopodia or woody rhizomes. Annual shoots sprout readily from the buds on these perennial woody organs, bearing leaves, inflorescences and fruits before they die back after the end of the rainy season. Coexistence of grasses and suffrutices is made possible by occupation of different ecological niches together with phase-delayed activity periods (i.e. main assimilation/flowering/fruiting time) that reduces competition.

Exploration of Geoxylic Grasslands

The first authors who indicated the distribution and ecological particularity of suffrutex-grasslands in Angola were Gossweiler and Mendonça (1939), who classified them as heathland-like woodlands (‘Ericilignosa’). They already noted the main differentiation between the Cryptosepalum spp. dominated suffrutex communities (‘Anharas de Ongote’) on ferralitic and psammoferralitic soils and the vegetation types characterised by Parinari capensis and the Apocynaceae Landolphia thollonii and L. camptoloba on leached sandy soils (‘Chanas da Borracha’). They had also already observed the strong thermic oscillations of which at least the ‘Anharas de Ongote’ are subject (see below) and commented on the generative cycle of Cryptosepalum maraviense from flowering to fruiting in the dry season (and thus, being inverse to the generative cycle of the C4-grasses).

Using a different mapping and classification approach, typical suffrutex-grasslands mostly on sandy soils were again mapped and described by Barbosa (1970) as ‘Chanas da Borracha’ (alluding to the presences of species of the genus Landolphia), ‘Chanas da Cameia’, and ‘Anharas do Alto’. The Cryptosepalum spp. dominated ‘Anharas de Ongote’ on ferralitic soils are described (but not depicted on the map) as being inserted in the main miombo types of the Angolan plateau. However, he describes the typical spatial pattern, i.e. how they appear close to the headwaters of the small tributaries and then follow the watercourses in narrow or broad fringes downstream. Gossweiler and Mendonça (1939) as well as Barbosa (1970), treated these ecosystems as particular site specific plant communities closely linked to woodland ecosystems, and not as grass-dominated savannas.

White (1983), however, mapped and described only the sandy ‘Chanas’ as ‘Kalahari and dambo-edge suffrutex grassland’ in the context of the ‘Zambezian edaphic grassland’, but did not refer to the ‘Anharas de Ongote’ which constitute a key (but small scale) element of the miombo ecosystems of the Angolan Plateau. Even in his prominent suffrutex review, White (1976) focuses solely on the ‘Chanas’ in the range of the Zambezi Graben and neither mentions (psammo-) ferralitic ‘Anharas’, nor lists their dominant key species Cryptosepalum maraviense and C. exfoliatum ssp. suffruticans in his suffrutex list. He certainly recognises a transition zone between Zambezian and Guineo-Congolian floras that spans over central and northern Angola (where the ‘Anharas’ are included) (White 1983). However, he did not recognise the importance and floristic singularity of the ferralitic suffrutex-grasslands dominated by Cryptosepalum spp.

Suffrutex Flora and Endemism

The suffrutex life form appears in many different floristic groups and obviously evolved convergently. A similar center of geoxyle diversity has been reported from the Brazilian Cerrado. Today, 198 species from 40 families are listed for the western Zambezian phytochorion (White 1976; Maurin et al. 2014, own data), but an even higher number is expected as floristic exploration of the region is still poor and new species might be found (see Goyder and Gonçalves 2019). In some cases suffrutices are considered a dwarf variety or subspecies of a closely related tree species (e.g. Gymnosporia senegalensis var. stuhlmanniana, Syzygium guineense ssp. huillense) and hence classified as such and not as one species, although the genetic relatedness between tree and dwarf form is rarely investigated. On the other hand, not all dwarf forms are obligate suffrutices; some can facultatively outgrow the dwarf state if protected from environmental stressors (White 1976), for instance Oldfieldia dactylophylla or Syzygium guineense ssp. macrocarpum (Zigelski et al. 2018).

Within the suffrutex communities of the Zambezian phytochorion, the Rubiaceae have the highest number of described taxa (46), followed by Anacardiaceae (22) and Lamiaceae (14). Table 7.1 lists all families with known geoxylic suffrutex taxa occurring in Angola and gives examples of common geoxyles for each family. Furthermore, Fig. 7.1 shows some examples and aspects of suffrutex species given in Table 7.1. The unique Zambezian geoxylic flora with a high number of endemic species (Brenan 1978; White 1983; Frost 1996) is a consequence of challenging environmental conditions, as illustrated further below. According to Figueiredo and Smith’s catalogue of Angolan plants (2008) and our list of suffrutices (Table 7.1), 121 of the 198 suffrutex species occurring in the Zambezian phytochorion are known from Angola (61%). Of these 121 species 12 are endemic to Angola (10%).
Table 7.1

List of plant families with geoxylic suffrutices in the Zambezian phytochorion

Plant family

Species common in Angola

Angolan endemics

Rubiaceae

46

Pygmaeothamnus zeyheri (Sond.) Robyns, Pachystigma pygmaeum (Schltr.) Robyns

2, e.g. Leptactina prostrata

Anacardiaceae

22

Lannea edulis (Sond.) Engl., Rhus arenaria Engl.

3, e.g. Lannea gossweileri

Lamiaceae

14

Clerodendrum ternatum Schinz, Vitex madiensis ssp. milanjensis (Britten) F.White

 

Fabaceae-Papilionioideae

13

Erythrina baumii Harms, Abrus melanospermum ssp. suffruticosus Hassk.

3, e.g. Adenodolichos mendesii

Proteaceae

11

Protea micans ssp. trichophylla (Engl. & Gilg) Chisumpa & Brummitt

1, Protea paludosa (Hiern) Engl.

Ochnaceae

9

Ochna arenaria De Wild. & T. Durand, Ochna manikensis De Wild.

 

Passifloraceae

7

Paropsia brazzaeana Baill.

 

Fabaceae-Detarioideae

6

Cryptosepalum maraviense Oliv., C. exfoliatum ssp. suffruticans (P.A.Duvign.)

 

Apocynaceae

5

Chamaeclitandra henriquesiana (Hallier f.) Pichon

1, Landolphia gossweileri

Ebenaceae

5

Diospyros chamaethamnus Mildbr, Euclea crispa (Thunb.) Gürke

 

Celastraceae

4

Gymnosporia senegalensis var. stuhlmanniana Loes.

 

Dichapetalaceae

4

Dichapetalum cymosum (Hook.) Engl.

 

Fabaceae-Caesalpinioideae

4

Entada arenaria Schinz

 

Myrtaceae

4

Syzygium guineense ssp. huillense, (Hiern) F. White Eugenia malangensis (O.Hoffm.) Nied.

 

Tiliaceae

4

Grewia herbaceae Hiern

 

Combretaceae

3

Combretum platypetalum Welw. ex M. A. Lawson

2, e.g. Combretum argyrotrichum

Euphorbiaceae

3

Sclerocroton oblongifolius (Müll.Arg.) Kruijt & Roebers

 

Loganiaceae

3

Strychnos gossweileri Exell

 

Annonaceae

2

Annona stenophylla ssp. nana (Exell) N. Robson

 

Apiaceae

2

Steganotaenia hockii (C. Norman) C. Norman

 

Chrysobalanaceae

2

Parinari capensis Harv., Magnistipula sapinii De Wild.

 

Meliaceae

2

Trichilia quadrivalvis C.DC.

 

Moraceae

2

Ficus pygmaea Welw. ex Hiern

 

Myricaceae

2

Morella serrata (Lam.) Killick

 

Phyllanthaceae

2

Phyllanthus welwitschianus Müll.Arg.

 

Ranunculaceae

2

Clematis villosa DC.

 

Achariaceae

1

Caloncoba suffruticosa (Milne-Redh.) Exell & Sleumer

 

Anisophyllaceae

1

Anisophyllea quangensis Engl. ex Henriq.

 

Clusiaceae

1

Garcinia buchneri Engl.

 

Dilleniaceae

1

Tetracera masuiana De Wild. & T. Durand

 

Fabaceae-Caesalpinioideae

1

Bauhinia mendoncae Torre & Hillc.

 

Hypericaceae

1

Psorosperum mechowii Engl.

 

Ixonanthaceae

1

Phyllocosmus lemaireanus (De Wild. & T. Durand) T. Durand & H. Durand

 

Lecythidaceae

1

Napoleonaea gossweileri Baker f.

 

Linaceae

1

Hugonia gossweileri Baker f. & Exell

 

Malpighiaceae

1

Sphedamnocarpus angolensis (A. Juss.) Planch. ex Oliv.

 

Malvaceae

1

Hibiscus rhodanthus Gürke

 

Melastomaceae

1

Heterotis canescens (E. Mey. ex Graham) Jacq.-Fél.

 

Picrodendraceae

1

Oldfieldia dactylophylla (Welw. ex Oliv.) J.Léonard

 

Rhamnaceae

1

Ziziphus zeyheriana Sond.

 

Urticaceae

1

Pouzolzia parasitica (Forssk.) Schweinf.

 

N°: overall number of Suffrutex species in the Zambezian phytochorion; examples of species occurring in Angola are given for each family. Compilation of families and species according to White (1976), Maurin et al. (2014) and own data

Fig. 7.1

Common Angolan suffrutex species. (a) Ochna arenaria (Ochnaceae), fruiting and growing on sandy sediments of the Bíe Plateau. (b) Syzygium guineense ssp. huillense (Myrtaceae) flowering in the dry season and growing on sandy soils of the Bíe Plateau. (c) Lannea edulis (Anacardiaceae), bearing edible fruits, growing on Kalahari sands in southeast Angola. (d) Hibiscus rodanthus (Malvaceae), growing on Kalahari sands in southeast Angola and flowering in the rainy season. (e) Landolphia gossweileri (Apocynaceae), typical element of the ‘Chanas da Borracha’, growing on sandy soils of the Bíe Plateau and bearing edible fruits. (f) Phyllanthus welwitschianus (Phyllanthaceae), growing on sandy soils of the Bíe Plateau and flowering in the rainy season. (g) Cryptosepalum exfoliatum ssp. suffruticans (Fabaceae – Detarioideae) with excavated rootstocks, typical element of the ‘Anharas de Ongote’, growing on psammoferralitic soils of the Bíe Plateau. (h) Parinari capensis (Chrysobalanaceae), typical element of the ‘Chanas da Borracha’, growing on slightly elevated termite mounds in flooded savannas of the Cameia National Park, Moxico Province

Environmental Conditions of Suffrutex-Grasslands Through the Year

The substrate strongly influences the species composition of the suffrutex-grasslands. In Angola geoxylic suffrutices occur on (a) well-drained arenosols which are found as seasonally flooded savannas in the Zambezi Graben of the Moxíco province or as sandy alluvial deposits on fossil river terraces along the valleys of the southern slopes of the Angolan plateau (Fig. 7.2a); (b) on psammo- ferralitic plinthisols as they frequently occur on the Bíe Plateau in central Angola. The suffrutex-grasslands on ferralitic soils mostly occur on mid- and foot-slopes and are embedded within a matrix of miombo woodland (Fig. 7.2b).
Fig. 7.2

Typical geoxylic suffrutex grasslands of Angola. (a) ‘Chanas da Cameia’ in the Cameia National Park, Moxíco Province, during dry season in June. The slightly elevated termite mounds provide habitat for several geoxyle species that avoid the low-lying areas that are waterlogged from January to May. (b) ‘Anharas de Ongote’ in the Sovi Valley on the southern slopes of the Bíe Plateau, in August. The mid- and footslopes are dominated by suffrutex-grassland with the characteristic reddish and green patches of the fresh leaves of Cryptosepalum maraviense, whereas the wetlands in the drainage lines are covered mostly by Cyperaceae (background, in dark green)

Environmental conditions in suffrutex-grasslands change dramatically throughout the year. The most perceived stresses are man-made fires in the dry season (May–October) which are mostly deployed to induce resprouting for livestock fodder or to facilitate hunting (Hall 1984). Depending on fire intensity, which in turn depends mostly on fuel load, ambient temperature and wind (Govender et al. 2006), such fires can completely burn unprotected aboveground biomass.

Another abiotic stress occurring mostly in the early dry season (June–August) is nocturnal frost, peaking immediately before sunrise. At this time of year masses of cold dry air from southern latitudes intrude into south-central Africa (Tyson and Preston-Whyte 2000). As depressions accumulate confluent cold air, the undulating topography of the Angolan highlands facilitates frequent radiation frost especially in valleys (Revermann and Finckh 2013; Finckh et al. 2016). Up to 44 frost events per dry season (with a minimum temperature of −7.5 °C) were recorded by Finckh et al. (2016), with a temperature span of up to 40 degrees within 12 h. Most woody species from tropical background (including geoxylic suffrutices) are sensitive to frost, their leaves wilt or their shoots die-off entirely.

The geoxylic suffrutex species seem to be triggered by the destruction of their shoots by frost and/or fire, as they readily resprout after these disturbances and in most cases already start flowering in the dry season. The suffrutices therefore have often already finished their generative cycle when the grasses start to cover them.

The suffrutex-grasslands of the sandy plains in eastern Angola are furthermore subject to seasonal flooding in the late rainy and early dry season (January–May), leading, for example, in the Cameia National Park to standing water up to 0.5 m deep. Whereas grass species dominate the sites which are inundated for several months, suffrutex species seem to avoid fully waterlogged sites and grow patchily on slightly elevated termite mounds (Fig. 7.2a) or other well drained sites.

The dominant grass species seem to profit from inundation. Their tufts develop massively in the middle of the rainy season and they flower and bear fruits throughout the flooding season (own observations).

Knowledge Gaps on the Evolution of the Geoxylic Suffrutices and the Formation of Suffrutex-Grasslands

A common observation within suffrutex ecosystems is the resemblance (Meerts 2017) and assumed close relatedness of suffrutex species to tree species that occur in forests and woodlands. The indigenous people (e.g. the Chokwe in eastern Angola) in many cases recognise the similarity and relatedness and use similar local names for such pairs, for instance Muhaua and Mupaua for the tree and suffrutex forms of Syzygium guineense Willd. DC. The striking fact that the suffrutex life form was developed by several plant families independently and at roughly the same time (Maurin et al. 2014) indicates a common driver that triggered its convergent evolution.

Grassy biomes emerged in Africa in the late Miocene approximately 10 mya (Cerling et al. 1997; Keeley and Rundel 2005; Herbert et al. 2016). This period is characterised by global climatic fluctuations which led to cooler, drier conditions, to a drop of atmospheric CO2 concentrations and particularly to pronounced precipitation seasonality (i.e. wet and dry seasons) in southern Africa (Pagani et al. 1999). As a consequence, humid tropical forests retreated to more favorable sites further north and were replaced by more open dry and seasonal tropical forest ecosystems like the miombo (Bonnefille 2011). In parts where miombo landscapes prevail today, canopies were disrupted and allowed the establishment of open ecosystems embedded in woodland matrices. These open ecosystems were then rapidly occupied by light-demanding C4-grasses and the evolving geoxylic suffrutices.

It is still an open discussion why open suffrutex-grasslands are able to persist within the woodlands (or vice versa). It is however likely that rainfall seasonality and the above described abiotic stresses that characterise the suffrutex-grasslands play a major role in their establishment and maintenance (Sankaran et al. 2005; Staver et al. 2011).

Savanna ecologists tend to see fire as the main driver for grassland formation. On the one hand frequent fires prevent tree establishment if saplings cannot outgrow the reach of the flames and are destroyed therein. For woodlands in eastern South Africa, a fire free time period of at least 5 years is necessary for many tree species to escape the ‘fire trap’ (Sankaran et al. 2004; Gignoux et al. 2009). This time window, allowing for successful reestablishment of trees, is rarely achieved in Angolan grasslands, at least nowadays (Schneibel et al. 2013; Stellmes et al. 2013). C4-savanna grasses, however, respond positively to periodic burning and resprout within weeks (Bond and Keeley 2005), thus being able to colonise seasonally burnt sites.

Forest ecologists, on the other hand, attribute the frequent short duration frost events in the dry season for preventing tree recruitment in the open areas (Finckh et al. 2016). As the list of suffrutices (Table 7.1) shows, mainly (but not exclusively) tropical families or genera evolved suffrutex life forms. Frost is deleterious to most tropical tree taxa, as they have not developed physiological adaptations to this ‘un-tropical’ stress factor, thus showing little or no frost tolerance (Sakai and Larcher 2012). As the suffrutex-grasslands are typically situated in particularly frost prone sites (depressions), tree taxa that are not adapted to frost are being filtered out of such environments.

In any case, a promising strategy to cope with seasonally returning thermic stress (by frost or fire) is to protect sensitive organs (buds) by hiding them underground. Tree species relocated their woody biomass and regenerative buds belowground at the expense of growth height and were thus able to cope with frost and fire prone sites (White 1976; Maurin et al. 2014; Finckh et al. 2016). Even shallow soil depths of less than 10 cm are sufficient to alleviate thermic stresses (Revermann and Finckh 2013). The high number of tropical genera and families that contribute to the suffrutex flora show how successful this strategy is for frost sensitive and fire susceptible taxa, in order to survive the adverse conditions of the open grasslands.

Concomitantly other evolutionary advantages of the geoxylic life form have been discussed, for instance poor edaphic conditions, as favoured by White (1976). He considered the low nutrient status of the leached and locally seasonal waterlogged soils on Kalahari sands as a likely cause for the lack of regular trees and the suffrutication of them as means of compensation. However, trees as well as suffrutices often grow on the same or similarly poor soils, with comparable physical and chemical properties (Gröngröft et al. 2013); forests and grasslands are not separated by edaphic boundaries but follow topographic rather than edaphic logics.

The waterlogging argument on the other hand would imply that the woody underground organs show adaptations to inundation, for instance aerenchymatic tissue or adventitious roots (Parolin 2008). Anatomical analyses of the rootstocks of four common suffrutex species however did not provide any support for aerenchymatic tissue nor other adaptations to inundation (Sanguino 2015). Moreover, in seasonally flooded savannas suffrutices avoid inundated sites. This is even the case for Syzygium guineense ssp. huillense, a suffrutex closely related to a tree species that grows along and in rivers and floodplains (Coates Palgrave 2002; Meerts and Hasson 2016).

To summarise, so far the main environmental driver for the astonishing radiation of geoxylic suffrutices has not been conclusively identified. The emergence of the suffrutex grassland at the end of the Pliocene and the peak of radiation at the beginning of the Pleistocene is clearly related to climatic seasonality and pronounced dry seasons. Dry seasons, however, did not only provide the necessary dry fuel for fire but also provided the atmospheric conditions for nocturnal frost events – the seasonality argument, thus, does not tip the balance toward fire or frost.

Conservation Value and Conservation Challenges

Various studies recognise the high floristic singularity of the Zambezian phytochorion and suffrutex-grasslands with its unique life forms contribute prominently to its high number of endemic species (Clayton and Cope 1980; White 1983). The high degree of suffrutex-grassland endemics within the Zambezian phytochorion as well as within Angola is a consequence of a unique setting of environmental drivers like nutrient poor soils, frequent frosts and fires or precipitation seasonality in a small-scale heterogeneous landscape (Linder 2001). Thus, the Zambezian phytochorion can be seen as an evolutionary laboratory that promoted the evolution of many specialised plant species, e.g. suffrutices, orchids and grasses.

Suffrutex-grasslands are sometimes misunderstood as ‘degraded forests’, overlooking their naturalness. Through this misconception they are listed as sites for reforestation in order to recover presumably lost forests and to sequestrate atmospheric CO2 (Parr et al. 2014). However, the well-intentioned act of reforestation would in fact destroy biodiverse natural ecosystems (Bond 2016). A lack of understanding, however, frustrates the development of appropriate conservation measures for the suffrutex grasslands today and in the future. The rebuilding process in Angola also has risks, happening at a rapid pace and shaping the landscape to human demands with limited consideration for sustainable management (Pröpper et al. 2015). Flooded savannas in the Moxíco Province for instance are targeted for large-scale agro-industrial development (ANGOP 2017). Not even National Parks offer adequate protection to ecosystems in this area, as the first rice schemes emerged during 2016 within the limits of Cameia National Park (own observation). Deficiencies in communication and cooperation between different ministries and governance levels aggravate such problems.

Outlook

Many questions still remain to be answered around the enigmatic life form of the geoxylic suffrutices. In order to efficiently safeguard suffrutex-grasslands, we need to understand the evolutionary drivers and evolutionary processes shaping these ecosystems. For instance, a thorough understanding of the evolutionary drivers and the response of suffrutices to them would help to assess how current environmental conditions affect the Zambezian ecosystems and how landscape shaping processes work. Moreover, investigations about genetic patterns of suffrutices and close tree-relatives would give insight to speciation processes, means of propagation (clonal or sexual) and evolutionary history. Also, ecophysiological or morphological measurements would contribute another perspective from which to assess how suffrutices react to environmental stresses and change processes. All these facets are currently the subjects of incipient research.

References

  1. ANGOP (2017) Cameia prepara mais de mil hectares para cultivar arroz. Agência Angola Press, Moxico, 16.07.2017. http://www.angop.ao/angola/pt_pt/noticias/economia/2017/6/28/Moxico-Cameia-prepara-mais-mil-hectares-para-cultivar-arroz,be825477-10c7-472d-b6e3-cb1ed5d25974.html. Accessed 22 Aug 2017
  2. Barbosa LAG (1970) Carta fitogeográfica de Angola. Instituto de Investigação Científica de Angola, LuandaGoogle Scholar
  3. Bond WJ (2016) Ancient grasslands at risk. Science 351(6269):120–122CrossRefGoogle Scholar
  4. Bond W, Keeley J (2005) Fire as a global ‘herbivore’: the ecology and evolution of flammable ecosystems. Trends Ecol Evol 20(7):387–394CrossRefGoogle Scholar
  5. Bonnefille R (2011) Rainforest responses to past climatic changes in tropical Africa. In: Tropical rainforest responses to climatic change. Springer, Berlin/Heidelberg, pp 125–184CrossRefGoogle Scholar
  6. Brenan JP (1978) Some aspects of the phytogeography of tropical Africa. Ann Mo Bot Gard 65(2):437–478CrossRefGoogle Scholar
  7. Cerling TE, Harris JM, MacFadden BJ et al (1997) Global vegetation change through the Miocene/Pliocene boundary. Nature 389(6647):153–158CrossRefGoogle Scholar
  8. Clayton WD, Cope TA (1980) The chorology of Old World species of Gramineae. Kew Bull 35(1):135–171CrossRefGoogle Scholar
  9. Coates Palgrave K (2002) Trees of southern Africa, 3rd edn. New edition revised and updated by Meg Coates Palgrave, Struik, Cape Town, pp 833–836Google Scholar
  10. Davy JB (1922) The suffrutescent habit as an adaptation to environment. J Ecol 10(2):211–219CrossRefGoogle Scholar
  11. Figueiredo E, Smith G (eds) (2008) Plants of Angola: Plantas de Angola. Strelitzia 22:1–279Google Scholar
  12. Finckh M, Revermann R, Aidar MP (2016) Climate refugees going underground–a response to Maurin et al. (2014). New Phytol 209(3):904–909CrossRefGoogle Scholar
  13. Frost P (1996) The ecology of miombo woodlands. In: Campbell B (ed) The Miombo in transition: woodlands and welfare in Africa. CIFOR, Jakarta, pp 11–57Google Scholar
  14. Gignoux J, Lahoreau G, Julliard R et al (2009) Establishment and early persistence of tree seedlings in an annually burned savanna. J Ecol 97(3):484–495CrossRefGoogle Scholar
  15. Gossweiler J, Mendonça FA (1939) Carta fitogeografica de Angola. Ministério das Colónias, Lisboa, p 242Google Scholar
  16. Govender N, Trollope WS, Van Wilgen BW (2006) The effect of fire season, fire frequency, rainfall and management on fire intensity in savanna vegetation in South Africa. J Appl Ecol 43(4):748–758CrossRefGoogle Scholar
  17. Goyder DJ, Gonçalves FPM (2019) The Flora of Angola: collectors, richness and endemism. In: Huntley BJ, Russo V, Lages F, Ferrand N (eds) Biodiversity of Angola. Science & conservation: a modern synthesis. SpringerGoogle Scholar
  18. Gröngröft A, Luther-Mosebach J, Landschreiber L et al (2013) Cusseque – soils. Biodivers Ecol 5:51–54CrossRefGoogle Scholar
  19. Hall M (1984) Man’s historical and traditional use of fire in southern Africa. In: de Booysen PV, Tainton NM (eds) Ecological effects of fire in South African ecosystems. Springer, Berlin/Heidelberg, pp 40–52Google Scholar
  20. Herbert TD, Lawrence KT, Tzanova A et al (2016) Late Miocene global cooling and the rise of modern ecosystems. Nat Geosci 9(11):843–847CrossRefGoogle Scholar
  21. Keeley JE, Rundel PW (2005) Fire and the Miocene expansion of C4 grasslands: miocene C4 grassland expansion. Ecol Lett 8(7):683–690CrossRefGoogle Scholar
  22. Linder HP (2001) Plant diversity and endemism in sub-Saharan tropical Africa. J Biogeogr 28(2):169–182CrossRefGoogle Scholar
  23. Maurin O, Davies TJ, Burrows JE et al (2014) Savanna fire and the origins of the ‘underground forests’ of Africa. New Phytol 204(1):201–214CrossRefGoogle Scholar
  24. Mayaux P, Bartholomé E, Fritz S et al (2004) A new land-cover map of Africa for the year 2000. J Biogeogr 31(6):861–877CrossRefGoogle Scholar
  25. Meerts P (2017) Geoxylic suffrutices of African savannas: short but remarkably similar to trees. J Trop Ecol 33(4):1–4CrossRefGoogle Scholar
  26. Meerts PJ, Hasson M (2016) Arbres et arbustes du Haut-Katanga. National Botanic Garden of BelgiumGoogle Scholar
  27. Pagani M, Freeman KH, Arthur MA (1999) Late Miocene atmospheric CO2 concentrations and the expansion of C4 grasses. Science 285(5429):876–879CrossRefGoogle Scholar
  28. Parolin P (2008) Submerged in darkness: adaptations to prolonged submergence by woody species of the Amazonian floodplains. Ann Bot 103(2):359–376CrossRefGoogle Scholar
  29. Parr CL, Lehmann CER, Bond WJ et al (2014) Tropical grassy biomes: misunderstood, neglected, and under threat. Trends Ecol Evol 29(4):205–213CrossRefGoogle Scholar
  30. Pröpper M, Gröngröft A, Finckh M et al (2015) The future Okavango: findings, scenarios and recommendations for action: research project final synthesis report 2010–2015. University of Hamburg-Biocentre Klein Flottbek, pp 53–129Google Scholar
  31. Revermann R, Finckh M (2013) Cusseque – micro-climatic conditions. Biodivers Ecol 5:47–50CrossRefGoogle Scholar
  32. Sakai A, Larcher W (2012) Frost survival of plants: responses and adaptation to freezing stress, vol 62. Springer, New York, pp 138–173CrossRefGoogle Scholar
  33. Sanguino G (2015) Wood anatomy and adaptation strategies of suffrutescent shrubs in South-Central Angola. MSc. thesis, Universität Hamburg, Hamburg, 68 ppGoogle Scholar
  34. Sankaran M, Ratnam J, Hanan NP (2004) Tree-grass coexistence in savannas revisited – insights from an examination of assumptions and mechanisms invoked in existing models. Ecol Lett 7(6):480–490CrossRefGoogle Scholar
  35. Sankaran M, Hanan NP, Scholes RJ et al (2005) Determinants of woody cover in African savannas. Nature 438(7069):846–849CrossRefGoogle Scholar
  36. Schneibel A, Stellmes M, Frantz D et al (2013) Cusseque – earth observation. Biodivers Ecol 5:55–57CrossRefGoogle Scholar
  37. Staver AC, Archibald S, Levin SA (2011) The global extent and determinants of savanna and forest as alternative biome states. Science 334(6053):230–232CrossRefGoogle Scholar
  38. Stellmes M, Frantz D, Finckh M et al (2013) Okavango basin – earth observation. Biodivers Ecol 5:23–27CrossRefGoogle Scholar
  39. Tyson PD, Preston-Whyte RA (2000) Weather and climate of Southern Africa, 2nd edn. Oxford University Press Southern Africa, Cape Town Chapter 10–12Google Scholar
  40. White F (1976) The underground forests of Africa: a preliminary review. Gard Bull Singap 29:57–71Google Scholar
  41. White F (1983) The Zambezian regional centre of endemism. In: White F (ed) The vegetation of Africa – a descriptive memoir to accompany the UNESCO/AETFAT/UNSO vegetation map of Africa. UNESCO, Paris, 356 ppGoogle Scholar
  42. Zigelski P, Lages F, Finckh M (2018) Seasonal changes of biodiversity patterns and habitat conditions in a flooded savanna – the Cameia National Park Biodiversity Observatory in the Upper Zambezi catchment, Angola. Biodivers Ecol 6:438–447CrossRefGoogle Scholar

Copyright information

© The Author(s) 2019

Open Access This chapter is licensed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license and indicate if changes were made.

The images or other third party material in this chapter are included in the chapter's Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the chapter's Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder.

Authors and Affiliations

  1. 1.Institute for Plant Science and MicrobiologyUniversity of HamburgHamburgGermany
  2. 2.Faculty of SciencesAgostinho Neto UniversityLuandaAngola

Personalised recommendations