Skip to main content
Log in

Inter- and intra-plant variations in nitrogen, tannins and shoot growth of Sclerocarya birrea browsed by elephants

  • Published:
Plant Ecology Aims and scope Submit manuscript

Abstract

Impacts of elephants (Loxodonta africana africana) on woody vegetation has attracted substantial attention for decades, but plant-level responses remain a gap in the understanding of savanna ecology. Marula (Sclerocarya birrea caffra) forms an important part of elephant diets. We investigated the relationships between browsing intensity and shoot/leaf size, nitrogen (N) and condensed tannin (CT) concentrations in upper and lower canopies of male and female marula individuals in Hluhluwe-iMfolozi Park, South Africa. Browsing intensity (54%) did not differ between sexes, suggesting no preference by elephants for either sex. Females had higher [CT] than males and tannin decreased with increasing browsing intensity in both sexes. In lightly or moderately browsed trees, [CT] was controlled by unmeasured factors such that within-tree impacts of browsing were more variable in lightly/moderately browsed than heavily browsed trees. There was little change in [N] up to ~60% browsing intensity, but [N] increased dramatically at higher intensity. Shoots and leaves on broken branches in the lower canopy were larger (2.5 and 1.2 times, respectively) than those on unbroken branches in either upper or lower canopies. Chemical responses were systemic and potentially influence browsing among trees, while growth responses were strongly localised and potentially influence browsing within trees. Although marula trees are able to compensate vigorously for browsing at the scale of individual organs, trees may become progressively carbon-deficient and have their lives shortened if total plant growth is negatively affected by chronic browsing, e.g. near permanent water.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Ågren GI (2008) Stoichiometry and nutrition of plant growth in natural communities. Ann Rev Ecol Evol Syst 39:153–170

    Article  Google Scholar 

  • Åhman I (1997) Growth, herbivory and disease in relation to gender in Salix viminalis L. Oecologia 111:61–68

    Article  Google Scholar 

  • AOAC (2000) Official methods of analysis, 16th edn. AOAC International, Gaithersburg

    Google Scholar 

  • Boundja RP, Midgley JJ (2010) Patterns of elephant impact on woody plants in the Hluhluwe-Imfolozi park, Kwazulu-Natal, South Africa. Afr J Ecol 48:206–214

    Article  Google Scholar 

  • Bryant JP, Heitkonig I, Kuropat P, Owen-Smith N (1991) Effects of severe defoliation on the long-term resistance to insect attack and on leaf chemistry in six woody species of the southern African savanna. Am Nat 137:50–63

    Article  Google Scholar 

  • Cade BS, Richards JD (2005) User manual for blossom statistical software. USGS, Virginia

    Google Scholar 

  • Coates Palgrave M (2005) Keith Coates Palgrave trees of southern Africa, 3rd edn. Struik Publishers, Cape Town

    Google Scholar 

  • Codron J, Codron D, Lee-Thorp JA, Sponheimer M, Kirkman K, Duffy KJ, Sealy J (2011) Landscape-scale feeding patterns of African elephant inferred from carbon isotope analysis of feces. Oecologia 165:89–99

    Article  PubMed  Google Scholar 

  • du Toit JT, Bryant JP, Frisby K (1990) Regrowth and palatability of Acacia shoots following pruning by African savanna browsers. Ecology 71:149–154

    Article  Google Scholar 

  • Fornara DA, du Toit JT (2007) Browsing lawns? Responses of Acacia nigrescens to ungulate browsing in an African savanna. Ecology 88:200–209

    Article  PubMed  CAS  Google Scholar 

  • Furstenburg D, van Hoven W (1994) Condensed tannin as anti-defoliate agent against browsing by giraffe (Giraffa camelopardalis) in the Kruger National Park. Comp Biochem Physiol 107A:425–431

    Article  CAS  Google Scholar 

  • Gadd ME (2002) The impact of elephants on the marula tree Sclerocarya birrea. Afr J Ecol 40:328–336

    Article  Google Scholar 

  • Gayler S, Grams TEE, Heller W, Treutter D, Priesack E (2007) A dynamical model of environmental effects on allocation to carbon-based secondary compounds in juvenile trees. Annal Bot 101:1089–1098

    Article  Google Scholar 

  • Glynn C, Herms DA, Orians CM, Hansen RC, Larsson S (2007) Testing the growth–differentiation balance hypothesis: dynamic responses of willows to nutrient availability. New Phytol 176:623–634

    Article  PubMed  CAS  Google Scholar 

  • Hagerman AE (2002) Tannin chemistry. Miami University, Oxford, Ohio, USA. http://www.users.muohio.edu/hagermae/tannin.pdf. Accessed 10 October 2010

  • Hagerman AE, Butler LG (1989) Choosing appropriate methods and standards for assaying tannin. J Chem Ecol 15:1795–1810

    Article  CAS  Google Scholar 

  • Helm CV, Witkowski ETF (2008) What don’t we know about Sclerocarya birrea subsp caffra? S Afr J Bot 74:387–388

    Article  Google Scholar 

  • Helm CV, Witkowski ETF, Kruger L, Hofmeyr M, Owen-Smith N (2009) Mortality and utilisation of Sclerocarya birrea subsp caffra between 2001 and 2008 in the Kruger National Park, South Africa. S Afr J Bot 75:475–484

    Article  Google Scholar 

  • Hemborg AM, Bond WJ (2007) Do browsing elephants damage female trees more? Afr J Ecol 45:41–48

    Article  Google Scholar 

  • Herms DA, Mattson WJ (1992) The dilemma of plants: to grow or defend. Q Rev Biol 67:283–335

    Article  Google Scholar 

  • Herrera CM (2009) Multiplicity in unity: plant subindividual variation and interactions with animals. University of Chicago Press, Chicago

    Google Scholar 

  • Hester AJ, Bergman M, Iason GR, Moen J (2006) Impacts of large herbivores on plant community structure and dynamics. In: Danell K, Bergström R, Duncan P, Pastor J (eds) Large herbivore ecology, ecosystem dynamics and conservation. Cambridge University Press, Cambridge, pp 97–141

    Chapter  Google Scholar 

  • Hrabar H, Hattas D, du Toit JT (2009) Differential effects of defoliation by mopane caterpillars and pruning by African elephants on the regrowth of Colophospermum mopane foliage. J Trop Ecol 25:301–309

    Article  Google Scholar 

  • Jachmann H, Bell RHV (1985) Utilization by elephants of the Brachystegia woodlands of the Kasungu-National-Park, Malawi. Afr J Ecol 23:245–258

    Article  Google Scholar 

  • Jacobs OS, Biggs R (2002a) The impact of the African elephant on marula trees in the Kruger National Park. S Afr J Wildl Res 32:13–22

    Google Scholar 

  • Jacobs OS, Biggs R (2002b) The status and population structure of the marula in the Kruger National Park. S Afr J Wildl Res 32:1–12

    Google Scholar 

  • Kerley GIH, Landman M, Kruger L, Owen Smith N (2008) Effects of elephants on ecosystems and biodiversity. In: Scholes RJ, Mennell KG (eds) Elephant management: a scientific assessment for South Africa. Wits University Press, Johannesburg, pp 146–205

    Google Scholar 

  • Li C, Trombley JD, Schmidt MA, Hagerman AE (2010) Preparation of an acid butanol standard from fresh apples. J Chem Ecol 36:453–460

    Article  PubMed  CAS  Google Scholar 

  • Makhabu SW, Skarpe C, Hytteborn H (2006) Elephant impact on shoot distribution on trees and on rebrowsing by smaller browsers. Acta Oecol 30:136–146

    Article  Google Scholar 

  • McNaughton SJ (1984) Grazing lawns: Animals in herds, plant form and coevolution. Am Nat 124:863–886

    Article  Google Scholar 

  • Mopipi K, Trollope WSW, Scogings PF (2009) Effects of moisture, nitrogen, grass competition and simulated browsing on the survival and growth of Acacia karroo seedlings. Afr J Ecol 47:680–687

    Article  Google Scholar 

  • Mucina L, Rutherford MC (2006) The vegetation of South Africa, Lesotho and Swaziland. South African National Biodiversity Institute, Pretoria

    Google Scholar 

  • Owen-Smith N (2002) Adaptive herbivore ecology. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Page BR (2005) Population structure, demographics and utilization—instructions for data capture. University of KwaZulu-Natal, Westville

    Google Scholar 

  • Pooley E (1994) The complete field guide to trees of Natal, Zululand & Transkei. Natal Flora Publications Trust, Durban

    Google Scholar 

  • Reich PB, Ellsworth DS, Walters MB (1998) Leaf structure (specific leaf area) modulates photosynthesis-nitrogen relations: evidence from within and across species and functional groups. Funct Ecol 12:948–958

    Article  Google Scholar 

  • Renton M, Thornby D, Hanan J (2007) Canonical modelling: an approach for intermediate-level simulation of carbon allocation in functional-structural plant models. In: Vos J, Marcelis LFM, de Visser PHB, Struik PC, Evers JB (eds) Functional-structural plant modelling in crop production. Springer, Dordrecht, pp 151–164

    Chapter  Google Scholar 

  • Rooke T, Bergström R (2007) Growth, chemical responses and herbivory after simulated leaf browsing in Combretum apiculatum. Plant Ecol 189:201–212

    Article  Google Scholar 

  • Scholes RJ, Bond WJ, Eckhardt HC (2003) Vegetation dynamics in the Kruger ecosystem. In: du Toit JT, Rogers KH, Biggs HC (eds) The Kruger experience. Island Press, Washington, pp 242–262

    Google Scholar 

  • Scogings PF, Macanda M (2005) Acacia karroo responses to early dormant season defoliation and debarking by goats in a semi-arid subtropical savanna. Plant Ecol 179:193–206

    Article  Google Scholar 

  • Scogings PF, Mopipi K (2008) Effects of water, grass and N on responses of Acacia karroo seedlings to early wet season simulated browsing: leaf N, fibre and tannin concentrations. J Arid Env 72:1666–1674

    Article  Google Scholar 

  • Scogings PF, Dziba LE, Gordon IJ (2004) Leaf chemistry of woody plants in relation to season, canopy retention and goat browsing in a semi-arid subtropical savanna. Austral Ecol 29:278–286

    Article  Google Scholar 

  • Scogings PF, Hjältén J, Skarpe C (2011) Secondary metabolites and nutrients of woody plants in relation to browsing intensity in African savannas. Oecologia. doi:10.1007/s00442-011-2042-9

  • Shrader AM, Bell C, Bertolli L, Ward D (2011) Forest or the trees: at what level do elephants make foraging decisions? Acta Oecol. doi:10.1016/j.actao.2011.09.009

  • Skarpe C, Hester AJ (2008) Plant traits, browsing and grazing herbivores, and vegetation dynamics. In: Gordon IJ, Prins HHT (eds) The ecology of browsing and grazing. Springer, Berlin, pp 217–261

    Chapter  Google Scholar 

  • Stuart-Hill GC, Tainton NM (1988) Browse and herbage production in the Eastern Cape thornveld in response to tree size and defoliation frequency. J Grassl Soc S Afr 5:42–47

    Article  Google Scholar 

  • SYSTAT Software (2007) SYSTAT 12. SYSTAT Software Inc., San Jose

    Google Scholar 

  • Teague WR (1988) Effect of the intensity and phenophase of defoliation and water stress on the rate of photosynthesis and the recovery of carbohydrate reserves in Acacia karroo Hayne. J Grassl Soc S Afr 5:223–226

    Article  Google Scholar 

  • Teague WR (1989) Effect of intensity and frequency of defoliation on aerial growth and carbohydrate reserve levels in Acacia karroo plants. J Grassl Soc S Afr 6:132–138

    Article  Google Scholar 

  • van Wyk B, van Oudtshoorn B, Gericke N (1997) Medicinal plants of South Africa. Briza Publications, Pretoria

    Google Scholar 

  • Ward D (2010) The effects of apical meristem damage on growth and defenses of two Acacia species in the Negev desert. Evol Ecol Res 12:589–602

    Google Scholar 

  • Ward D, Young TP (2002) Effects of large mammalian herbivores and ant symbionts on condensed tannins of Acacia drepanolobium in Kenya. J Chem Ecol 28:913–929

    Google Scholar 

  • Wessels DCJ, van der Waal C, de Boer WF (2007) Induced chemical defences in Colophospermum mopane trees. Afr J Range Forage Sci 24:141–147

    Article  Google Scholar 

Download references

Acknowledgments

The National Research Foundation, University of Zululand and University of KwaZulu-Natal provided financial support. Bruce Page contributed to designing the methods. Dave Druce provided logistical support. Douglas Makin, Megan Welsford, Tiffany Pillay, Vanessa Stuart and Desale Okubamichael helped in the field and lab. The comments from three anonymous reviewers improved the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Peter F. Scogings.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Scogings, P.F., Taylor, R.W. & Ward, D. Inter- and intra-plant variations in nitrogen, tannins and shoot growth of Sclerocarya birrea browsed by elephants. Plant Ecol 213, 483–491 (2012). https://doi.org/10.1007/s11258-011-9996-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11258-011-9996-x

Keywords

Navigation