Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Frankincense in peril

Nature Sustainability volume 2, pages 602–610 (2019)Cite this article

Subjects

Abstract

The harvest of plant parts and exudates from wild populations contributes to the income, food security and livelihoods of many millions of people worldwide. Frankincense, an aromatic resin sourced from natural populations of Boswellia trees and shrubs, has been cherished by world societies for centuries. Boswellia populations are threatened by over-exploitation and ecosystem degradation, jeopardizing future resin production. Here, we reveal evidence of population collapse of B. papyrifera—now the main source of frankincense—throughout its geographic range. Using inventories of 23 populations consisting of 21,786 trees, growth-ring data from 202 trees and demographic models on the basis of 7,246 trees, we find that over 75% of studied populations lack small trees, natural regeneration has been absent for decades, and projected frankincense production will be halved in 20 yr. These changes are caused by increased human population pressure on Boswellia woodlands through cattle grazing, frequent burns and reckless tapping. A literature review showed that other Boswellia species experience similar threats. Populations can be restored by establishing cattle exclosures and fire-breaks, and by planting trees and tapping trees more carefully. Concerted conservation and restoration efforts are urgently needed to secure the long-term availability of this iconic product.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Distribution of major frankincense-producing species and main threats to existing populations.
Fig. 2: Distribution and size structures of Boswellia papyrifera populations.
Fig. 3: Regeneration failure in Boswellia populations obtained from tree-ring analysis.
Fig. 4: Projected development of Boswellia populations and frankincense yield at 23 sites.

Similar content being viewed by others

Data availability

The data reported in this paper are tabulated in the Supplementary Data and can be accessed in the Github repository (https://github.com/groenendijk/Frankincense-demography).

Code availability

The R script used for the IPM analysis can be accessed in the Github repository (https://github.com/groenendijk/Frankincense-demography).

References

  1. Hamilton, A. C. Medicinal plants, conservation and livelihoods. Biodivers. Conserv. 13, 1477–1517 (2004).

    Article  Google Scholar 

  2. Ticktin, T. The ecological implications of harvesting non-timber forest products. J. Appl. Ecol. 41, 11–21 (2004).

    Article  Google Scholar 

  3. Godfray, H. C. J. et al. Food security: the challenge of feeding 9 billion people. Science 327, 812 (2010).

    Article  CAS  Google Scholar 

  4. Millenium Ecosystem Assessment Ecosystems and Human Well-being: Synthesis (Island Press, 2005).

  5. Peres, C. A. et al. Demographic threats to the sustainability of Brazil nut exploitation. Science 302, 2112–2114 (2003).

    Article  CAS  Google Scholar 

  6. Groom, N. Frankincense and Myrrh. A Study of the Arabian Incense Trade (Longman, 1981).

  7. Alaamri, M. M. H. Distribution Boswellia sacra in Dhofar mountains, Sultanate of Oman: economic values and environmental role. J. Life Sci. 6, 632–636 (2012).

    Google Scholar 

  8. DeCarlo, A. & Ali, S. H. Sustainable Sourcing of Phytochemicals as a Development Tool: The Case of Somaliland’s Frankincense Industry (Institute for Environmental Diplomacy & Security, 2014).

  9. Kushwaha, C. P. & Singh, K. P. Diversity of leaf phenology in a tropical deciduous forest in India. J. Trop. Ecol. 21, 47–56 (2005).

    Article  Google Scholar 

  10. Singh, K. P. & Kushwaha, C. P. Diversity of flowering and fruiting phenology of trees in a tropical deciduous forest in India. Ann. Bot. 97, 265–276 (2006).

    Article  CAS  Google Scholar 

  11. Sagar, R. & Singh, J. S. Tree density, basal area and species diversity in a disturbed dry tropical forest of northern India: implications for conservation. Environ. Conserv. 33, 256 (2006).

    Article  Google Scholar 

  12. Brendler, T., Brinckmann, J. A. & Schippmann, U. Sustainable supply, a foundation for natural product development: the case of Indian frankincense (Boswellia serrata Roxb. ex Colebr.). J. Ethnopharmacol. 225, 279–286 (2018).

    Article  CAS  Google Scholar 

  13. Groenendijk, P., Eshete, A., Sterck, F. J., Zuidema, P. A. & Bongers, F. Limitations to sustainable frankincense production: blocked regeneration, high adult mortality and declining populations. J. Appl. Ecol. 49, 164–173 (2012).

    Article  Google Scholar 

  14. Zewdie, W. & Csaplovies, E. Remote sensing based multi-temporal land cover classification and change detection in northwestern Ethiopia. Eur. J. Remote Sens. 48, 121–139 (2015).

    Article  Google Scholar 

  15. Lemenih, M., Arts, B., Wiersum, K. F. & Bongers, F. Modelling the future of Boswellia papyrifera population and its frankincense production. J. Arid Environ. 105, 33–40 (2014).

    Article  Google Scholar 

  16. Gezahgne, A., Yirgu, A. & Kassa, H. Morphological characterization of fungal disease on tapped Boswellia papyrifera trees in Metema and Humera Districts, Northern Ethiopia. Ethiop. J. Agric. Sci. 27, 89–98 (2017).

    Google Scholar 

  17. Negussie, A. et al. An exploratory survey of long horn beetle damage on the dryland flagship tree species Boswellia papyrifera (Del.) Hochst. J. Arid Environ. 152, 6–11 (2018).

    Article  Google Scholar 

  18. Ogbazghi, W. The Distribution and Regeneration of Boswellia papyrifera (Del.) Hochst. in Eritrea. PhD thesis, Wageningen Univ. (2001).

  19. Ogbazghi, W., Rijkers, T., Wessel, M. & Bongers, F. Distribution of the frankincense tree Boswellia papyrifera in Eritrea: the role of environment and land use. J. Biogeogr. 33, 524–535 (2006).

    Article  Google Scholar 

  20. Khamis, M. A., Siddig, E. N. E., Khalil, A. & Csaplovics, E. Changes in forest cover composition of Boswellia papyrifera (Del.) Hochst. stands and their consequences, South Kordofan, Sudan. Mediterr. J. Biosci. 1, 99–108 (2016).

    Google Scholar 

  21. Tolera, M., Sass-Klaassen, U., Eshete, A., Bongers, F. & Sterck, F. J. Frankincense tree recruitment failed over the past half century. For. Ecol. Manag. 304, 65–72 (2013).

    Article  Google Scholar 

  22. Zuidema, P. A., Jongejans, E., Chien, P. D., During, H. J. & Schieving, F. Integral Projection Models for trees: a new parameterization method and a validation of model output. J. Ecol. 98, 345–355 (2010).

    Article  Google Scholar 

  23. Rijkers, T., Ogbazghi, W., Wessel, M. & Bongers, F. The effect of tapping for frankincense on sexual reproduction in Boswellia papyrifera. J. Appl. Ecol. 43, 1188–1195 (2006).

    Article  Google Scholar 

  24. Teshome, M., Eshete, A. & Bongers, F. Uniquely regenerating frankincense tree populations in western Ethiopia. For. Ecol. Manage. 389, 127–135 (2017).

    Article  Google Scholar 

  25. Eshete, A., Sterck, F. J. & Bongers, F. Frankincense production is determined by tree size and tapping frequency and intensity. For. Ecol. Manage. 274, 136–142 (2012).

    Article  Google Scholar 

  26. Tilahun, M. et al. Frankincense yield assessment and modeling in closed and grazed Boswellia papyrifera woodlands of Tigray, Northern Ethiopia. J. Arid Environ. 75, 695–702 (2011).

    Article  Google Scholar 

  27. Hansen, M. C. et al. High-resolution global maps of 21st-century forest cover change. Science 342, 850–853 (2013).

    Article  CAS  Google Scholar 

  28. Melo, J. B. et al. Striking divergences in Earth Observation products may limit their use for REDD+. Environ. Res. Lett. 13, 104020 (2018).

    Article  Google Scholar 

  29. Criteria for Amendment of Appendices I and II. Resolution Conf. 9.24 (Rev. CoP17) (CITES, 2016); https://cites.org/sites/default/files/document/E-Res-09-24-R17.pdf

  30. Holmgren, M. & Scheffer, M. El Niño as a window of opportunity for the restoration of degraded arid ecosystems. Ecosystems 4, 151–159 (2001).

    Article  Google Scholar 

  31. Tierney, J. E., Ummenhofer, C. C. & deMenocal, P. B. Past and future rainfall in the Horn of Africa. Sci. Adv. 1, e1500682 (2015).

    Article  Google Scholar 

  32. Seleshi, Y. & Zanke, U. Recent changes in rainfall and rainy days in Ethiopia. Int. J. Climatol. 24, 973–983 (2004).

    Article  Google Scholar 

  33. Segele, Z. T., Richman, M. B., Leslie, L. M. & Lamb, P. J. Seasonal-to-interannual variability of Ethiopia/Horn of Africa monsoon. Part II: Statistical multimodel ensemble rainfall predictions. J. Clim. 28, 3511–3536 (2015).

    Article  Google Scholar 

  34. van Breugel, P., Friis, I., Demissew, S., Barnekow Lillesø, J. P. & Kindt, R. Current and future fire regimes and their influence on natural vegetation in Ethiopia. Ecosystems 19, 369–386 (2016).

    Article  Google Scholar 

  35. Mengistu, T., Sterck, F. J., Fetene, M. & Bongers, F. Frankincense tapping reduces the carbohydrate storage of Boswellia trees. Tree Physiol. 33, 601–608 (2013).

    Article  CAS  Google Scholar 

  36. Abiyu, A. et al. in Degraded Forests in Eastern Africa: Management and Restoration (eds Bongers, F. & Tennigkeit, T.) 133–152 (Earthscan, 2010).

  37. Birhane, E., Kuyper, T. W., Sterck, F. J., Gebrehiwot, K. & Bongers, F. Arbuscular mycorrhiza and water and nutrient supply differently impact seedling performance of dry woodland species with different acquisition strategies. Plant Ecol. Divers. 8, 387–399 (2015).

    Article  Google Scholar 

  38. Lemenih, M. & Kassa, H. Management Guide for Sustainable Production of Frankincense (CIFOR, 2011).

  39. Mekuria, W., Veldkamp, E., Tilahun, M. & Olschewski, R. Economic valuation of land restoration: the case of exclosures established on communal grazing lands in Tigray, Ethiopia. Land Degrad. Dev. 22, 334–344 (2011).

    Article  Google Scholar 

  40. Lemenih, M. & Kassa, H. Re-greening Ethiopia: history, challenges and lessons. Forests 5, 1896–1909 (2014).

    Article  Google Scholar 

  41. Mekuria, W. & Veldkamp, E. Restoration of native vegetation following exclosure establishment on communal grazing lands in Tigray, Ethiopia. Appl. Veg. Sci. 15, 71–83 (2012).

    Article  Google Scholar 

  42. Haile, G., Gebrehiwot, K., Lemenih, M. & Bongers, F. Time of collection and cutting sizes affect vegetative propagation of Boswellia papyrifera (Del.) Hochst through leafless branch cuttings. J. Arid Environ. 75, 873–877 (2011).

    Article  Google Scholar 

  43. Negussie, A., Aerts, R., Gebrehiwot, K., Prinsen, E. & Muys, B. Euphorbia abyssinica latex promotes rooting of Boswellia cuttings. New For. (Dordr.) 37, 35–42 (2008).

    Google Scholar 

  44. Kassa, H., Tefera, B. & Fitwi, G. Preliminary Value Chain Analysis of Gum and Resin Marketing in Ethiopia. Issues for Policy and Research (CIFOR, 2011).

  45. Hardin, G. The tragedy of the commons. Science 162, 1243–1248 (1968).

    Article  CAS  Google Scholar 

  46. Dietz, T., Ostrom, E. & Stern, P. The struggle to govern the commons. Science 302, 1907–1912 (2003).

    Article  CAS  Google Scholar 

  47. Tilahun, M., Maertens, M., Deckers, J., Muys, B. & Mathijs, E. Impact of membership in frankincense cooperative firms on rural income and poverty in Tigray, Northern Ethiopia. For. Policy Econ. 62, 95–108 (2016).

    Article  Google Scholar 

  48. Agrawal, A., Chhatre, A. & Hardin, R. Changing governance of the world’s forests. Science 320, 1460–1462 (2008).

    Article  CAS  Google Scholar 

  49. Al-Aamri, M. M. Sustainable Harvesting of Frankincense Trees in Oman (Environment Society of Oman, 2014).

  50. Al-Harrasi, A. et al. Chemical, molecular and structural studies of Boswellia species: beta-Boswellic aldehyde and 3-epi-11beta-dihydroxy BA as precursors in biosynthesis of boswellic acids. PLoS ONE 13, e0198666 (2018).

    Article  Google Scholar 

  51. Khan, A. L. et al. The first chloroplast genome sequence of Boswellia sacra, a resin-producing plant in oman. PLoS ONE 12, e0169794 (2017).

    Article  Google Scholar 

  52. Khan, A. L. et al. Regulation of endogenous phytohormones and essential metabolites in frankincense-producing Boswellia sacra under wounding stress. Acta Physiol. Plant. 40, 113 (2018).

    Article  Google Scholar 

  53. Khan, A. L., Asaf, S., Al-Rawahi, A., Lee, I. J. & Al-Harrasi, A. Rhizospheric microbial communities associated with wild and cultivated frankincense producing Boswellia sacra tree. PLoS ONE 12, e0186939 (2017).

    Article  Google Scholar 

  54. DeCarlo, A., Elmi, A. D. & Johnson, S. Sustainable Frankincense Production Systems in Somaliland. A Management Guide (Conserve the Cal Madow, 2017).

  55. Standard for Good Field Collection Practices of Medicinal Plants (NMPB, Department of AYUSH, Ministry of Health and Family Welfare, Government of India, 2009).

  56. Mishra, S., Behera, N. & Paramanik, T. Comparative assessment of gum yielding capacities of Boswellia serrata Roxb. and Sterculia urens Roxb. in relation to their girth sizes. Ecoscan 1, 327–330 (2012).

    Google Scholar 

  57. Schweingruber, F. H, Börner, A. & Schulze, E. D. Atlas of Woody Plant Stems: Evolution, Structure and Environmental Modifications (Springer-Verlag, 2006).

  58. Rinn, F. TSAP-Win Software for Tree-ring Measurement Analysis and Presentation (Rinntech, 2003).

  59. Schweingruber, F. H. Tree Rings: Basics and Applications of Dendrochronology (Kluwer Academic, 1988).

  60. Eshete, A., Sterck, F. J. & Bongers, F. Diversity and production of Ethiopian dry woodlands explained by climate- and soil-stress gradients. For. Ecol. Manage. 261, 1499–1509 (2011).

    Article  Google Scholar 

  61. Baker, T. R., Affum-Baffoe, K., Burslem, D. F. R. P. & Swaine, M. D. Phenological differences in tree water use and the timing of tropical forest inventories: conclusions from patterns of dry season diameter change. For. Ecol. Manage. 171, 261–274 (2002).

    Article  Google Scholar 

  62. Chitra-Tarak, R. et al. And yet it shrinks: a novel method for correcting bias in forest tree growth estimates caused by water-induced fluctuations. For. Ecol. Manage. 336, 129–136 (2015).

    Article  Google Scholar 

  63. Zweifel, R., Haeni, M., Buchmann, N. & Eugster, W. Are trees able to grow in periods of stem shrinkage? New Phytol. 211, 839–849 (2016).

    Article  Google Scholar 

  64. R Core Team. R: A language and environment for statistical computing. (R Foundation for Statistical Computing, 2018); http://www.R-project.org/

  65. Bates, D., Maechler, M., Bolker, B. & Walker, S. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67, 1–48 (2015).

    Article  Google Scholar 

  66. Ellner, S. P. & Rees, M. Integral projection models for species with complex demography. Am. Nat. 167, 410–428 (2006).

    Article  Google Scholar 

  67. Kroon, Hd, Groenendael, Jv & Ehrlen, J. Elasticities: a review of methods and model limitations. Ecology 81, 607–618 (2000).

    Article  Google Scholar 

  68. Metcalf, C. J. E., McMahon, S. M., Salguero-Gómez, R. & Jongejans, E. IPMpack: an R package for integral projection models. Methods Ecol. Evol. 4, 195–200 (2013).

    Article  Google Scholar 

Download references

Acknowledgements

This work is part of the FRAME integrated programme (‘Frankincense, myrrh and arabic gum: sustainable use of dry woodland resources in Ethiopia’). A large part of this programme was financially supported by Netherlands Organisation for Scientific Research-Science for Global Development (NWO-WOTRO, grant no. W01.65.220.00). Additional support was received from: a SIDA grant to M.Tol., BES grants 2732/3420 to M.Tol. and 1415/1782 to E.B., Wageningen University Sandwich grants to E.B., M.Tol. and W.O., IFS grant C/4775-1 to M.Tol., NUFFIC grant CF6676/2010 to E.B. and Marie Curie Actions Programme grant PITN-2013-GA607545 to P.G. P.G. was also supported by FAPESP grant 18/01847-0.

Author information

Author notes

  1. These authors contributed equally: Frank J. Sterck, Pieter A. Zuidema.

Authors and Affiliations

  1. Forest Ecology and Forest Management Group, Wageningen University and Research, Wageningen, the Netherlands

    Frans Bongers, Peter Groenendijk, Mathieu Decuyper, Ute Sass-Klaassen, Frank J. Sterck & Pieter A. Zuidema

  2. Departamento de Botánica, Escola Politécnica Superior, Campus de Lugo, Universidade de Santiago de Compostela, Lugo, Spain

    Peter Groenendijk

  3. Department of Plant Biology, Institute of Biology, University of Campinas, Campinas, Brazil

    Peter Groenendijk

  4. Ethiopian Environment and Forest Research Institute, Addis Ababa, Ethiopia

    Tesfaye Bekele, Abeje Eshete, Alemu Gezahgne, Wubalem Tadesse & Mindaye Teshome

  5. Department of Land Resources Management and Environmental protection, Mekelle University, Mekelle, Ethiopia

    Emiru Birhane, Abebe Damtew & Atkilt Girma

  6. Department of Ecology and Natural Resource Management, Norwegian University of Life Sciences, Ås, Norway

    Emiru Birhane

  7. Geo-Information and Remote Sensing Group, Wageningen University and Research, Wageningen, the Netherlands

    Mathieu Decuyper

  8. ITC faculty, University of Twente, Enschede, the Netherlands

    Atkilt Girma

  9. Department of Forestry and Range Sciences, University of Al Fashir, Al Fashir, Sudan

    Mohamed A. Khamis

  10. Farm Africa, Regional office, Addis Ababa, Ethiopia

    Mulugeta Lemenih

  11. Forest Sector Development Program, UNDP/MEFCC, Addis Ababa, Ethiopia

    Tefera Mengistu

  12. University of Asmara, Asmara, Eritrea

    Woldeselassie Ogbazghi

  13. Wondo Genet College of Forestry and Natural Resources, Hawassa University, Shashemene, Ethiopia

    Motuma Tolera

Authors
  1. Frans Bongers
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Peter Groenendijk
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Tesfaye Bekele
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Emiru Birhane
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Abebe Damtew
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Mathieu Decuyper
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Abeje Eshete
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Alemu Gezahgne
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Atkilt Girma
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Mohamed A. Khamis
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Mulugeta Lemenih
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Tefera Mengistu
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Woldeselassie Ogbazghi
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Ute Sass-Klaassen
    View author publications

    You can also search for this author in PubMed Google Scholar

  15. Wubalem Tadesse
    View author publications

    You can also search for this author in PubMed Google Scholar

  16. Mindaye Teshome
    View author publications

    You can also search for this author in PubMed Google Scholar

  17. Motuma Tolera
    View author publications

    You can also search for this author in PubMed Google Scholar

  18. Frank J. Sterck
    View author publications

    You can also search for this author in PubMed Google Scholar

  19. Pieter A. Zuidema
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

F.B., F.J.S., P.A.Z. and P.G. conceived the study. F.B. and P.G. compiled the data. P.G. and P.A.Z. performed the demographic modelling. M.D. evaluated forest change. F.B., P.A.Z., F.J.S. and P.G. wrote the paper. All authors contributed data and commented on the manuscript.

Corresponding author

Correspondence to Frans Bongers.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Supplementary Information

Supplementary Figs. 1–8, Supplementary Tables 1–5, Supplementary method 1, Supplementary Note 1, Supplementary References 1–12

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bongers, F., Groenendijk, P., Bekele, T. et al. Frankincense in peril. Nat Sustain 2, 602–610 (2019). https://doi.org/10.1038/s41893-019-0322-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41893-019-0322-2

This article is cited by

Search

Advanced search

Quick links

Nature Briefing Anthropocene

Sign up for the Nature Briefing: Anthropocene newsletter — what matters in anthropocene research, free to your inbox weekly.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing: Anthropocene