What shapes the range edge of a dominant African savanna tree, Colophospermum mopane? A demographic approach

Abstract Climate is widely assumed to be the primary process that limits the distribution ranges of plants. Yet, savannas have vegetation not at equilibrium with climate, instead its structure and function are shaped by interactions between fire, herbivory, climate, and vegetation. I use the rich literature of a dominant African savanna woody plant, Colophospermum mopane, to demonstrate that climate and disturbance interact with each demographic stage to shape this species range limits. This synthesis highlights that climate‐based predictions for the range of C. mopane inadequately represents the processes that shape its distribution. Instead, seed bank depletion and rainfall limitation create a demographic bottleneck at the early seedling stage. The legacy of top‐kill from disturbance changes tree stand architecture causing a critical limitation in seed supply. Exposure to top‐kill at all demographic stages causes a vigorous resprouting response and shifts tree architecture from that of 1–2 stemmed tall trees to that of a short multi‐stemmed shrub. The shorter, multi‐stemmed shrubs are below the height threshold (4 m) at which they can produce seeds, resulting in shrub‐dominated landscapes that are effectively sterile. This effect is likely most pronounced at the range edge where top‐kill‐inducing disturbances increase in frequency. The proposed mechanistic, demographic‐based understanding of C. mopane's range limits highlights the complexity of processes that interact to shape its range edges. This insight serves as a conceptual model for understanding the determinants of range limits of other dominant woody savannas species living in disturbance limited ecosystems.

[1]  D. Wiggins Fluctuating asymmetry in Colophospermum mopane leaves and oviposition preference in an African silk moth Imbrasia belina , 1997 .

[2]  Ana Luz,et al.  Charcoal production in the Mopane woodlands of Mozambique: what are the trade-offs with other ecosystem services? , 2016, Philosophical Transactions of the Royal Society B: Biological Sciences.

[3]  J. Timberlake,et al.  A review of the significance of mopane products to rural people's livelihoods in southern Africa , 2014 .

[4]  J. Gambiza,et al.  Fire‐tolerance mechanisms of common woody plant species in a semiarid savanna in south‐western Zimbabwe , 2007 .

[5]  H. Hrabar,et al.  Differential effects of defoliation by mopane caterpillars and pruning by African elephants on the regrowth of Colophospermum mopane foliage , 2009, Journal of Tropical Ecology.

[6]  K. Gaston Geographic range limits: achieving synthesis , 2009, Proceedings of the Royal Society B: Biological Sciences.

[7]  W. Bond,et al.  A synthesis of the demography of African acacias , 2001, Journal of Tropical Ecology.

[8]  E. Kohi,et al.  Effects of simulated browsing on growth and leaf chemical properties in Colophospermum mopane saplings. , 2010 .

[9]  W. Bond,et al.  Fire frequency filters species by bark traits in a savanna–forest mosaic , 2017 .

[10]  R. Ben-Shahar Patterns of elephant damage to vegetation in northern Botswana , 1993 .

[11]  G. N. Smit,et al.  THE INFLUENCE OF TREE THINNING ON THE REPRODUCTION DYNAMICS OF COLOPHOSPERMUM MOPANE , 1998 .

[12]  G. Midgley,et al.  Photosynthetic and gas exchange characteristics of dominant woody plants on a moisture gradient in an African savanna , 2004 .

[13]  S. Levin,et al.  The Global Extent and Determinants of Savanna and Forest as Alternative Biome States , 2011, Science.

[14]  S. Moe,et al.  What controls woodland regeneration after elephants have killed the big trees , 2009 .

[15]  G. N. Smit,et al.  Root biomass, depth distribution and relations with leaf biomass of Colophospermum mopane , 1998 .

[16]  F. Siebert A phytosociological synthesis of Mopanieveld vegetation at different spatial scales using various classification methods , 2012 .

[17]  W. Bond,et al.  Corrigendum to: A handbook for the standardised sampling of plant functional traits in disturbance-prone ecosystems, with a focus on open ecosystems , 2020, Australian Journal of Botany.

[18]  D. Wessels,et al.  Floral development in the legume tree Colophospermum mopane, Caesalpinioideae: Detarieae , 1999 .

[19]  F. I. Woodward,et al.  Climate and plant distribution at global and local scales , 1987, Vegetatio.

[20]  I. Mapaure The distribution of colophospermum mopane (Leguminosae-caesalpinioideae) in Africa , 1994 .

[21]  D. Wessels,et al.  Structure of the style and wet non-papillate stigma of Colophospermum mopane, Caesalpinioideae: Detarieae , 2002 .

[22]  D. Ward,et al.  Herbivory effects on saplings are influenced by nutrients and grass competition in a humid South African savanna , 2014 .

[23]  J. Ott,et al.  Coping with herbivory at the juvenile stage: responses to defoliation and stem browsing in the African savanna tree Colophospermum mopane , 2012, Journal of Tropical Ecology.

[24]  H. Krüger,et al.  Development and functional anatomy of pods of Colophospermum mopane (Caesalpinioideae: Dietarieae) , 2005 .

[25]  Molotja M. Georginah,et al.  Assessment of plant biodiversity on and off mature stands of Androstachys johnsonii Prain and Colophospermum mopane (J.Kirk ex Benth.) J. Leonard , 2015 .

[26]  S. Archibald,et al.  Do freeze events create a demographic bottleneck for Colophospermum mopane , 2012 .

[27]  C. Ryan,et al.  Ecosystem services from southern African woodlands and their future under global change , 2016, Philosophical Transactions of the Royal Society B: Biological Sciences.

[28]  N. Fairall,et al.  The influence of the African Elephant on the vegetation of the Kruger National Park , 1969 .

[29]  Stephan Getzin,et al.  Walter’s two-layer hypothesis revisited: back to the roots! , 2012, Oecologia.

[30]  A. Bennett The Origin of Species by means of Natural Selection; or the Preservation of Favoured Races in the Struggle for Life , 1872, Nature.

[31]  D. Ward,et al.  Shade, nutrients, and grass competition are important for tree sapling establishment in a humid savanna , 2013 .

[32]  B. Walker,et al.  The Effects of Different Forms of Land Use on the Ecology of a Semi-Arid Region in South-Eastern Rhodesia , 1976 .

[33]  K. Gaston,et al.  Changing size and changing enemies: the case of the mopane worm , 1997 .

[34]  J. Dudley Seed Dispersal by Elephants in Semiarid Woodland Habitats of Hwange National Park, Zimbabwe1 , 2000 .

[35]  G. Caughley The elephant problem–an alternative hypothesis , 1976 .

[36]  J. Choinski,et al.  Effect of Water Potential and Temperature on the Germination of Four Species of African Savanna Trees , 1991 .

[37]  Simon Scheiter,et al.  Effects of four decades of fire manipulation on woody vegetation structure in Savanna. , 2007, Ecology.

[38]  S. Higgins,et al.  When is a ‘forest’ a savanna, and why does it matter? , 2011 .

[39]  T. O’Connor Woody vegetation–environment relations in a semi-arid savanna in the northern Transvaal , 1992 .

[40]  Pierre Hiernaux,et al.  Savanna Vegetation-Fire-Climate Relationships Differ Among Continents , 2014, Science.

[41]  I. Mapaure,et al.  Post-fire resprouting of Colophospermum mopane saplings in a southern African savanna , 2006, Journal of Tropical Ecology.

[42]  Patrick J. McIntyre,et al.  Evolution and Ecology of Species Range Limits , 2009 .

[43]  T. O’Connor,et al.  Elephant utilization of Colophospermum mopane: possible benefits of hedging , 2000 .

[44]  E. Gandiwa,et al.  Influence of fire frequency on Colophospermum mopane and Combretum apiculatum woodland structure and composition in northern Gonarezhou National Park, Zimbabwe , 2009 .

[45]  J. Poulsen,et al.  Ecological consequences of forest elephant declines for Afrotropical forests , 2018, Conservation biology : the journal of the Society for Conservation Biology.

[46]  A. Viljoen The influence of the 1991/92 drought on the woody vegetation of the Kruger National Park , 1995 .

[47]  R. E. White,et al.  A study of the growth and distribution of Colophospermum mopane (Kirk ex Benth.) Kirk ex J. Leon: the interaction of nitrogen phosphorus and soil moisture stress , 1974 .

[48]  R. Scholes,et al.  Evidence for facultative deciduousness in Colophospermum mopane in semi-arid African savannas , 2016 .

[49]  D. Richardson,et al.  Determinants of Plant Distribution: Evidence from Pine Invasions , 1991, The American Naturalist.

[50]  W. Luus‐Powell,et al.  Factors influencing the adaptation and distribution of Colophospermum mopane in southern Africa’s mopane savannas – A review , 2014 .

[51]  Christopher N. Johnson,et al.  Combining paleo-data and modern exclosure experiments to assess the impact of megafauna extinctions on woody vegetation , 2015, Proceedings of the National Academy of Sciences.

[52]  R. Ben-Shahar Woodland dynamics under the influence of elephants and fire in Northern Botswana , 1996, Vegetatio.

[53]  W. Bond,et al.  Increasing temperatures can improve seedling establishment in arid-adapted savanna trees , 2014, Oecologia.

[54]  N. Stevens Exploring the potential impacts of global change on the woody component of of South African savannas , 2014 .

[55]  D. Wessels,et al.  The aril of Colophospermum mopane. Its role during seed germination and fruit opening , 1999 .

[56]  A. D. Tomos,et al.  Growth, water relations and solute accumulation in osmotically stressed seedlings of the tropical tree Colophospermum mopane. , 1996, Tree physiology.

[57]  P. Bruschi,et al.  Traditional knowledge on ethno-veterinary and fodder plants in South Angola: an ethnobotanic field survey in Mopane woodlands in Bibala, Namibe province , 2017 .

[58]  J. Midgley,et al.  Mass sterilization of a common palm species by elephants in Kruger National Park, South Africa , 2020, Scientific Reports.

[59]  W. F. Boer,et al.  The diet of kudus in a mopane dominated area, South Africa , 2005 .

[60]  P. P. Smith,et al.  An investigation into the relationship between physical damage and fungal infection in Colophospermum mopane , 1999 .

[61]  C. Ryan,et al.  Carbon losses from deforestation and widespread degradation offset by extensive growth in African woodlands , 2018, Nature Communications.

[62]  A. D. Kennedy,et al.  Fire season affects size and architecture of Colophospermum mopane in southern African savannas , 2003, Plant Ecology.

[63]  W. Bond,et al.  Humboldt and the reinvention of nature , 2018, Journal of Ecology.

[64]  M. Picker Field Guide to Insects of South Africa , 2002 .

[65]  Teresa J. Feo,et al.  Structural absorption by barbule microstructures of super black bird of paradise feathers , 2018, Nature Communications.

[66]  T. O’Connor,et al.  Patch dieback of Colophospermum mopane in a dysfunctional semi‐arid African savanna , 2002 .

[67]  B. Walker,et al.  VEGETATION-ENVIRONMENT RELATIONS ON SODIC SOILS OF ZIMBABWE RHODESIA , 1980 .

[68]  G. Smit The influence of tree thinning on the vegetative growth and browse production of Colophospermum mopane , 2001 .

[69]  M. Hoffman,et al.  Bush encroachment in southern Africa: changes and causes , 2014 .

[70]  I. Mapaure,et al.  Patterns of elephant damage to colophospermum mopane on selected islands in Lake Kariba, Zimbabwe , 2000 .

[71]  Kimberly S. Sheldon Climate Change in the Tropics: Ecological and Evolutionary Responses at Low Latitudes , 2019, Annual Review of Ecology, Evolution, and Systematics.

[72]  W. Bond,et al.  Transplant Experiments Point to Fire Regime as Limiting Savanna Tree Distribution , 2018, Front. Ecol. Evol..

[73]  William J. Bond,et al.  What Limits Trees in C4 Grasslands and Savannas , 2008 .

[74]  H. J. de Knegt,et al.  Water and nutrients alter herbaceous competitive effects on tree seedlings in a semi‐arid savanna , 2009 .

[75]  J. Skinner,et al.  The influence of large mammalian herbivores on growth form and utilization of mopane trees, Colophospermum mopane, in Botswana's Northern Tuli Game Reserve. , 2000 .

[76]  R. Ben-Shahar Do elephants over-utilize mopane woodlands in northern Botswana? , 1996, Journal of Tropical Ecology.

[77]  K. Esler,et al.  Fire and life history affect the distribution of plant species in a biodiversity hotspot , 2019, Diversity and Distributions.

[78]  J. Nippert,et al.  Savanna Tree Seedlings are Physiologically Tolerant to Nighttime Freeze Events , 2016, Front. Plant Sci..

[79]  Stephen P. Hubbell,et al.  Reproductive size thresholds in tropical trees: variation among individuals, species and forests , 2005, Journal of Tropical Ecology.

[80]  R. Macarthur Mathematical Ecology and Its Place among the Sciences. (Book Reviews: Geographical Ecology. Patterns in the Distribution of Species) , 1974 .

[81]  N. Ribeiro,et al.  Biodiversity Studies in Key Species from the African Mopane and Miombo Woodlands , 2017 .

[82]  G. Smit,et al.  Browse production and leaf phenology of some trees and shrubs in different Colophospermum mopane savanna communities , 1996 .

[83]  J. Manning,et al.  Allozyme variation in five populations of mopane, Colophospermum mopane (Fabaceae) , 2003 .

[84]  Barend F.N. Erasmus,et al.  Investigating potential determinants of the distribution limits of a savanna woody plant: Colophospermum mopane , 2014 .

[85]  S. Higgins,et al.  Fire, resprouting and variability: a recipe for grass–tree coexistence in savanna , 2000 .

[86]  J. Skinner,et al.  Mopane diaspores are not dispersed by epizoochory , 1997 .

[87]  Jean Clobert,et al.  Alternative fire resistance strategies in savanna trees , 1997, Oecologia.

[88]  Helena De Nagy Koves Hrabar Indirect interactions between elephants (Loxodonta africana) and mopane caterpillars (Imbrasia belina) through their shared food resource – mopane trees (Colophospermum mopane) , 2007 .

[89]  P. Nyathi,et al.  Seedling recruitment of Colophospermum mopane on the Highveld of Zimbabwe , 2004 .

[90]  S. Okitsu FACTORS CONTROLLING GEOGRAPHICAL DISTRIBUTION IN SAVANNA VEGETATION IN NAMIBIA , 2005 .

[91]  R. Bergström,et al.  Morphological responses of woody species to simulated twig-browsing in Botswana , 2004, Journal of Tropical Ecology.

[92]  D. Lewis Observations of tree growth, woodland structure and elephant damage on Colophospermum mopane in Luangwa Valley, Zambia , 1991 .

[93]  F. Woodward,et al.  The global distribution of ecosystems in a world without fire. , 2004, The New phytologist.

[94]  H. Banks,et al.  Pollen morphology and wood anatomy of the Crudia group (Leguminosae, Caesalpinioideae, Detarieae) , 2000 .

[95]  C. Donaldson Goats and/or cattle on Mopani veld , 1979 .

[96]  A. Burke Savanna trees in Namibia—Factors controlling their distribution at the arid end of the spectrum , 2006 .

[97]  F. Woodward Climate and plant distribution , 1987 .