Landscape Ecology

, Volume 30, Issue 10, pp 2161–2174 | Cite as

Termite mounds mitigate against 50 years of herbivore-induced reduction of functional diversity of savanna woody plants

  • Grant S. Joseph
  • Milton Makumbe
  • Colleen L. Seymour
  • Graeme S. Cumming
  • Zacheus Mahlangu
  • David H. M. Cumming
Research Article



Spatially heterogeneous habitats often promote woody plant species and functional diversity (FD). Ungulate herbivory can have the opposite effect. Across the globe, the type and intensity of herbivory is changing, as domestic livestock replace wild ungulates, which are increasingly confined to protected areas. Despite recognition of the importance of FD for ecosystem functioning, the interactive effect of soil-related fine-scale heterogeneity and larger-scale ungulate herbivory on woody plant FD is little-known.


In miombo woodland of Zimbabwe, we investigated (1) how bottom-up fine-scale heterogeneity created by Macrotermes termitaria interacts with top-down effects of herbivore foraging-guilds on woody plant FD; and (2) whether browsing combined with grazing impacts FD more than grazing alone.


The three different herbivore treatments (grazing, combined browsing-and-grazing, and exclusion) had been maintained for 50 years. We surveyed 10 termite mound-matrix plots within three sites per treatment. We assessed woody plant traits and FD across treatments (herbivore feeding-guild) and position (mound or woodland-matrix), and interactive effects between these.


Woody plant FD was greater on mounds, and lowest overall with browsing-and-grazing. Specific traits were associated with position (e.g. palatability was greater for mounds), and treatment (e.g. spinescence increased with grazing).


Long-term enclosure of ungulate herbivores (browsing-and-grazing, and grazing alone) decreased woody FD, but this was mitigated by termitaria. The novel finding is that at regional scales, mounds can enhance woody plant FD despite the impacts of herbivory. At broader scales encompassing the miombo system, potential exists for mounds to stabilise woody plant FD from livestock-induced impacts.


Bottom-up versus top-down effects Functional divergence Functional evenness Functional richness Spatial heterogeneity Termitaria 


  1. Aerts R (1995) The advantages of being evergreen. Trends Ecol Evol 10:402–407CrossRefPubMedGoogle Scholar
  2. Anderson JP, Brin PJ, Moyo M, Nyamawanza B (1993) Physical resource inventory of the communal lands of Zimbabwe—an overview. NRI Bulletin 60. Natural Resources Institute, ChathamGoogle Scholar
  3. Augustine DJ, McNaughton SJ (1998) Ungulate effects on the functional species composition of plant communities: herbivore selectivity and plant tolerance. J Wildl Manage 62:1165–1183CrossRefGoogle Scholar
  4. Bakker ES, Ritchie ME, Olff H, Milchunas DG, Knops JMH (2006) Herbivore impact on grassland plant diversity depends on habitat productivity and herbivore size. Ecol Lett 9:780–788. doi:10.1111/j.1461-0248.2006.00925.x CrossRefPubMedGoogle Scholar
  5. Bonachela JA, Pringle RM, Sheffer E, Coverdale TC, Guyton JA, Caylor KK, Levin SA, Tarnita CE (2015) Termite mounds can increase the robustness of dryland ecosystems to climatic change. Science 347:651–655CrossRefPubMedGoogle Scholar
  6. Carmona CP, Azcárate FM, de Bello F, Ollero HS, Lepš J, Begoña P (2012) Taxonomical and functional diversity turnover in Mediterranean grasslands: interactions between grazing, habitat type and rainfall. J Appl Ecol 49:1084–1093. doi:10.1111/j.1365-2664.2012.02193.x CrossRefGoogle Scholar
  7. Child MF, Milton SA, Dean WRJ, Lipsey MK, Puttick J, Hempson TN, Mann GK, Babiker H, Chaudrey J, Humphrey G, Joseph G, Okes NC, Potts R, Wistebaar T (2010) Tree-grass coexistence in a flood-disturbed, semi-arid savanna system. Landsc Ecol 25:315–326. doi:10.1007/s10980-009-9409.x CrossRefGoogle Scholar
  8. Coe MJ, Cumming DH, Phillipson J (1976) Biomass and production of large Africa herbivores in relation to rainfall ands primary production. Oecologia 22:341–354CrossRefGoogle Scholar
  9. Colwell RK (2006) EstimateS: statistical estimation of species richness and shared species from samples. Version 8. User’s Guide and application published at:
  10. Colwell RK, Coddington JA (1994) Estimating terrestrial biodiversity through extrapolation. Philos Trans R Soc Lond B 345:101–118CrossRefGoogle Scholar
  11. Connell JH (1978) Diversity in tropical rain forests and coral reefs. Science 199:1302–1310CrossRefPubMedGoogle Scholar
  12. Cornelissen JHC, Lavorel S, Garnier E, Díaz S, Buchmann N, Gurvich DE, Reich PB, ter Steege H, Morgan HD, Van Der Heijden MGA, Pausas JG, Poorter H (2003) A handbook of protocols for standardised and easy measurement of plant functional traits worldwide. Aust J Bot 51:335–380. doi:10.1071/BT02124 CrossRefGoogle Scholar
  13. Cumming DHM (1982) The influence of large herbivores on savanna structure in Africa. In: Huntley B, Walker BH (eds) Ecology of tropical savannas. Springer, Berlin, pp 217–245CrossRefGoogle Scholar
  14. Cumming DHM, Cumming GS (2003) Ungulate community structure and ecological processes: body size, hoof area and trampling in African savannas. Oecologia 134:560–568CrossRefPubMedGoogle Scholar
  15. Davies AB, Robertson MP, Levick SR, Asner GP, van Rensburg BJ, Parr CL (2014) Variable effects of termite mounds on African savanna grass communities across a rainfall gradient. J Veg Sci 25:1405–1416. doi:10.1111/jvs.12200 CrossRefGoogle Scholar
  16. Díaz S, Cabido M (2001) Vive la différence : plant functional diversity matters to ecosystem processes. Trends Ecol Evol 16:646–655CrossRefGoogle Scholar
  17. Du Toit JT, Bryant JP, Frisby K (1990) Regrowth and palatability of Acacia shoots following pruning by African savanna browsers. Ecology 71:149–154CrossRefGoogle Scholar
  18. Dukes JS (2001) Biodiversity and invasibility in grassland microcosms. Oecologia 126:563–568CrossRefGoogle Scholar
  19. Ehlers Smith YC, Ehlers Smith DA, Seymour CL, Thébault E, van Veen FJF (2015) Response of avian diversity to habitat modification can be predicted from life-history traits and ecological attributes. Landsc Ecol 30:1225–1239. doi:10.1007/s10980-015-0172-x CrossRefGoogle Scholar
  20. Erpenbach A, Wittig R, Hahn K (2014) Dynamics of juvenile woody plant communities on termite mounds in a West African savanna landscape. Flora Veg Sudano-Sambesica 17:28–41Google Scholar
  21. Ettema CH, Wardle DA (2002) Spatial soil ecology. Trends Ecol Evol 17:177–183CrossRefGoogle Scholar
  22. Frost P (1996) The ecology of miombo woodlands. In: Campbell B (ed) Miombo transit. Woodlands and welfare in Africa. Center for International Forestry Research (CIFOR), Bogor, pp 11–58Google Scholar
  23. Garnier E, Cortez J, Billès G, Navas M-L, Roumet C, Debussche M, Laurent G, Blanchard A, Aubry D, Belllmmann A, Neill C, Toussaint J-P (2004) Plant functional markers capture ecosystem properties during secondary succession. Ecology 85:2630–2637CrossRefGoogle Scholar
  24. Higgins SI, Bond WJ, February EC, Bronn A, Euston-Brown DIW, Enslin B, Govender N, Rademan L, O’ Regan S, Potgieter ALF, Scheiter S, Sowry R, Trollope L, Trollope WSW (2007) Effects of four decades of fire manipulation on woody vegetation structure in savanna. Ecology 88:1119–1125CrossRefPubMedGoogle Scholar
  25. Hunter MD, Price PW (1992) Playing chutes and ladders: heterogeneity and the relative roles of bottom-up and top-down forces in natural communities. Ecology 73:724–732Google Scholar
  26. Huntley BJ (1982) Southern African savannas. In: Huntley BJ, Walker BH (eds) Ecology of tropical savannas. Springer-Verlag, Berlin, pp 101–119CrossRefGoogle Scholar
  27. Jacobs S, Bechtold J, Biggs H, Grimm N, Lorentz S, McClain M, Naiman R, Perakis S, Pinay G, Scholes M (2007) Nutrient vectors and riparian processing: a review with special reference to African semiarid savanna ecosystems. Ecosystems 10:1231–1249CrossRefGoogle Scholar
  28. Joseph GS, Cumming GS, Cumming DHM, Mahlangu Z, Altwegg R, Seymour CL (2011) Large termitaria act as refugia for tall trees, deadwood and cavity-using birds in a miombo woodland. Landsc Ecol 26:439–448. doi:10.1007/s10980-011-9572-8 CrossRefGoogle Scholar
  29. Joseph GS, Seymour CL, Cumming GS, Cumming DHM, Mahlangu Z (2012) Termite mounds as islands: woody plant assemblages relative to termitarium size and soil properties. J Veg Sci 24:702–711. doi:10.1111/j.1654-1103.2012.01489.x CrossRefGoogle Scholar
  30. Joseph GS, Seymour CL, Cumming GS, Mahlangu Z, Cumming DHM (2013) Escaping the flames: large termitaria as refugia from fire in miombo woodland. Landsc Ecol 28:1505–1516. doi:10.1007/s10980-013-9897-6 CrossRefGoogle Scholar
  31. Joseph GS, Seymour CL, Cumming GS, Cumming DHM, Mahlangu Z (2014) Termite mounds increase functional diversity of woody plants in African savannas. Ecosystems 17:808–819. doi:10.1007/s10021-014-9761-9 CrossRefGoogle Scholar
  32. Kraaij T, Ward D (2006) Effects of rain, nitrogen, fire and grazing on tree recruitment and early survival in bush-encroached savanna, South Africa. Plant Ecol 186:235–246. doi:10.1007/s11258-006-9125-4 CrossRefGoogle Scholar
  33. Laliberté E, Shipley B (2011) FD: measuring functional diversity from multiple traits, and other tools for functional ecology. R package 1.0-11. R-CRAN, ViennaGoogle Scholar
  34. Lavorel S, Grigulis K, McIntyre S, Williams NSG, Garden D, Dorrough J, Berman S, Quétier F, Thébault A, Bonis A (2008) Assessing functional diversity in the field—methodology matters! Funct Ecol 22:134–147. doi:10.1111/j.1365-2435.2007.01339.x Google Scholar
  35. Levick SR, Asner GP, Kennedy-Bowdoin T, Knapp DE (2010) The spatial extent of termite influences on herbivore browsing in an African savanna. Biol Conserv 143:2462–2467. doi:10.1016/j.biocon.2010.06.012 CrossRefGoogle Scholar
  36. Loveridge JP, Moe SR (2004) Termitaria as browsing hotspots for African megaherbivores in miombo woodland. J Trop Ecol 20:337–343. doi:10.1017/S0266467403001202 CrossRefGoogle Scholar
  37. Malaisse F (1978) High termitaria. In: Werger MJA (ed) Biogeography and ecology of southern Africa. Junk, The Hague, pp 1279–1300CrossRefGoogle Scholar
  38. Mason NWH, Mouillot D, Lee WG, Wilson JB (2005) Functional richness, functional evenness and functional divergence : the primary components of functional diversity. Oikos 1:112–118CrossRefGoogle Scholar
  39. Mason NWH, Peltzer DA, Richardson SJ, Bellingham PJ, Allen RB (2010) Stand development moderates effects of ungulate exclusion on foliar traits in the forests of New Zealand. J Ecol 98:1422–1433. doi:10.1111/j.1365-2745.2010.01714.x CrossRefGoogle Scholar
  40. Mobæk R, Narmo AK, Moe SR (2005) Termitaria are focal feeding sites for large ungulates in Lake Mburo National Park, Uganda. J Zool 267:97–102. doi:10.1017/S0952836905007272 CrossRefGoogle Scholar
  41. Moleele NM, Ringrose S, Matheson W, Vanderpost C (2002) More woody plants? The status of bush encroachment in Botswana’s grazing areas. J Environ Manag 64:3–11CrossRefGoogle Scholar
  42. Mouchet MA, Villéger S, Mason NWH, Mouillot D (2010) Functional diversity measures: an overview of their redundancy and their ability to discriminate community assembly rules. Funct Ecol 24:867–876. doi:10.1111/j.1365-2435.2010.01695.x CrossRefGoogle Scholar
  43. O’Connor TG, Roux PW (1995) Vegetation changes (1949–71) in a semi-arid, grassy dwarf shrubland in the Karoo, South Africa: influence of rainfall variability and grazing by sheep. J Appl Ecol 32:612–626CrossRefGoogle Scholar
  44. Okullo P, Moe SR (2012) Termite activity, not grazing, is the main determinant of spatial variation in savanna herbaceous vegetation. J Ecol 100:232–241. doi:10.1111/j.1365-2745.2011.01889.x CrossRefGoogle Scholar
  45. Podani J (1999) Extending Gower’s general coefficient of similarity to ordinal characters. Taxon 48:331–340CrossRefGoogle Scholar
  46. Podani J, Schmera D (2006) On dendrogram-based measures of functional diversity. Oikos 115:179–185CrossRefGoogle Scholar
  47. Pringle RM, Doak DF, Brody AK, Jocqué R, Palmer TM (2010) Spatial pattern enhances ecosystem functioning in an African savanna. PLoS Biol 8:e1000377. doi:10.1371/journal.pbio.1000377 PubMedCentralCrossRefPubMedGoogle Scholar
  48. Proulx M, Mazumder A (1998) Reversal of grazing impact on plant species richness in nutrient-poor vs. nutrient-rich ecosystems. Ecology 79:2581–2592CrossRefGoogle Scholar
  49. Richardson-Kageler SJ (2003) Large mammalian herbivores and woody plant species diversity in Zimbabwe. Biodivers Conserv 12:703–715CrossRefGoogle Scholar
  50. Richardson-Kageler SJ (2004) Effects of large herbivore browsing on the functional groups of woody plants in a southern African savanna. Biodivers Conserv 13:2145–2163CrossRefGoogle Scholar
  51. Sankaran M, Ratnam J (2013) African and Asian Savannas. Encycl Biodivers 1:58–74CrossRefGoogle Scholar
  52. Sankaran M, Ratnam J, Hanan N (2008) Woody cover in African savannas: the role of resources, fire and herbivory. Glob Ecol Biogeogr 17:236–245. doi:10.1111/j.1466-8238.2007.00360.x CrossRefGoogle Scholar
  53. Schleuter D, Daufresne M, Massol F, Argillier C (2010) A user’s guide to functional diversity indices. Ecol Monogr 80:469–484CrossRefGoogle Scholar
  54. Seif El Din A, Obeid M (1971) Ecological studies of the vegetation of the Sudan. IV. The effect of simulated grazing on the growth of Acacia senegal (L.) Willd. seedlings. J Appl Ecol 8:211–216CrossRefGoogle Scholar
  55. Seymour CL (2008) Grass, rainfall and herbivores as determinants of Acacia erioloba (Meyer) recruitment in an African savanna. Plant Ecol 197:131–138. doi:10.1007/s11258-007-9366-x CrossRefGoogle Scholar
  56. Seymour CL, Dean WRJ (2010) The influence of changes in habitat structure on the species composition of bird assemblages in the southern Kalahari. Aust Ecol 35:581–592. doi:10.1111/j.1442-9993.2009.02069.x CrossRefGoogle Scholar
  57. Seymour CL, Milton SJ, Joseph GS, Dean WRJ, Ditlhobolo T, Cumming GS (2010) Twenty years of rest returns grazing potential, but not palatable plant diversity, to Karoo rangeland, South Africa. J Appl Ecol 47:859–867. doi:10.1111/j.1365-2664.2010.01833.x CrossRefGoogle Scholar
  58. Seymour CL, Milewski AV, Mills AJ, Joseph GS, Cumming GS, Cumming DHM, Mahlangu Z (2014) Do the large termite mounds of Macrotermes concentrate micronutrients in addition to macronutrients in nutrient-poor African savannas? Soil Biol Biochem 68:95–105. doi:10.1016/j.soilbio.2013.09.022 CrossRefGoogle Scholar
  59. Seymour CL, Simmons RE, Joseph GS, Slingsby JA (2015) On bird functional diversity: species richness and functional differentiation show contrasting responses to rainfall and vegetation structure in an arid landscape. Ecosystems. doi:10.1007/s10021-015-9875-8 Google Scholar
  60. Skinner JD, Chimimba CT (2005) The Mammals of the Southern African Subregion, 3rd Editio. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  61. Stein A, Gerstner K, Kreft H (2014) Environmental heterogeneity as a universal driver of species richness across taxa, biomes and spatial scales. Ecol Lett. doi:10.1111/ele.12277 Google Scholar
  62. Taylor RD, Walker BH (1978) A comparison of vegetation use and condition in relation to herbivore biomass on a Rhodesian game and cattle ranch. J Appl Ecol 15:565–581CrossRefGoogle Scholar
  63. Thompson JG (1965) Rhodesian soils. In: Rhodesia; its natural resources and economic development. M.O. Collins (Pvt.) Ltd., Salisbury, pp 24–25Google Scholar
  64. Tilman D (1996) Biodiversity : population versus ecosystem stability. Ecology 77:350–363CrossRefGoogle Scholar
  65. Torrance JD (1965) The temperature of Rhodesia. In: Collins MO (ed) Rhod. its Nat. Resour. Econ. Dev. pp 28–29Google Scholar
  66. Veblen KE, Young TP (2010) Contrasting effects of cattle and wildlife on the vegetation development of a savanna landscape mosaic. J Ecol 98:993–1001. doi:10.1111/j.1365-2745.2010.01705.x CrossRefGoogle Scholar
  67. Walker BH (1980) A review of browse and its role in livestock production in southern African savannas. Proc Grassl Soc South Africa 11:125–130CrossRefGoogle Scholar
  68. Weiher E, Keddy P (1999) Assembly rules as general constraints on community composition. In: Weiher E, Keddy P (eds) Ecological assembly rules. Cambridge University Press, Cambridge, pp 251–271CrossRefGoogle Scholar
  69. Wigley BJ, Fritz H, Coetsee C, Bond WJ (2014) Herbivores shape woody plant communities in the Kruger National Park: lessons from three long-term exclosures. Koedoe 56(1):1–12CrossRefGoogle Scholar
  70. Young TP, Okello B, Kinyua D, Palmer TM (1997) KLEE: a long-term multi-species herbivore exclusion experiment in Laikipia, Kenya. African J Range Forage Sci 14:94–102. doi:10.1080/10220119.1997.9647929 CrossRefGoogle Scholar
  71. Young HS, McCauley DJ, Helgen KM, Goheen JR, Otárola-Castillo E, Palmer TM, Pringle RM, Young TP, Dirzo R (2013) Effects of mammalian herbivore declines on plant communities: observations and experiments in an African savanna. J Ecol 101:1030–1041. doi:10.1111/1365-2745.12096 PubMedCentralCrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2015

Authors and Affiliations

  • Grant S. Joseph
    • 1
  • Milton Makumbe
    • 3
  • Colleen L. Seymour
    • 1
    • 2
  • Graeme S. Cumming
    • 1
    • 4
  • Zacheus Mahlangu
    • 3
  • David H. M. Cumming
    • 1
    • 3
  1. 1.Percy FitzPatrick Institute of African Ornithology, DST/NRF Centre of Excellence, Department of Biological SciencesUniversity of Cape TownCape TownSouth Africa
  2. 2.South African National Biodiversity InstituteKirstenbosch Research CentreCape TownSouth Africa
  3. 3.Tropical Resource Ecology Programme, Department of Biological SciencesUniversity of ZimbabweHarareZimbabwe
  4. 4.ARC Centre of Excellence for Coral Reef StudiesJames Cook UniversityTownsvilleAustralia

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