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.

Elephant genotypes reveal the size and connectivity of transnational ivory traffickers

Nature Human Behaviour volume 6, pages 371–382 (2022)Cite this article

Subjects

Abstract

Transnational ivory traffickers continue to smuggle large shipments of elephant ivory out of Africa, yet prosecutions and convictions remain few. We identify trafficking networks on the basis of genetic matching of tusks from the same individual or close relatives in separate shipments. Analyses are drawn from 4,320 savannah (Loxodonta africana) and forest (L. cyclotis) elephant tusks, sampled from 49 large ivory seizures totalling 111 t, shipped out of Africa between 2002 and 2019. Network analyses reveal a repeating pattern wherein tusks from the same individual or close relatives are found in separate seizures that were containerized in, and transited through, common African ports. Results suggest that individual traffickers are exporting dozens of shipments, with considerable connectivity between traffickers operating in different ports. These tools provide a framework to combine evidence from multiple investigations, strengthen prosecutions and support indictment and prosecution of transnational ivory traffickers for the totality of their crimes.

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

Access options

Rent or buy this article

Get just this article for as long as you need it

$39.95

Learn more

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

Fig. 1: Geographical span and colour code scheme for ports of containerization used for all consequent figures.
Fig. 2: Temporal progression in the major ports of containerization and their connectivity, based on genetic matches and shared physical evidence between seizures.
Fig. 3: Genetic and physical-evidence matches between tusks in representative ivory seizures containerized in East Africa and all other seizures in our dataset.
Fig. 4: Seizures containerized in West Africa.
Fig. 5: Network of all genetic matches between seizures.

Data availability

DNA sequences have been deposited in GenBank (accession numbers OK382584–OK382941; http://www.ncbi.nlm.nih.gov/nucest?term=OK382584:OK2941). Data related to this paper may be requested from the authors. However, ivory samples and genetic data derived from them are subject to restricted access (see https://obamawhitehouse.archives.gov/the-press-office/2014/02/11/fact-sheet-national-strategy-combating-wildlife-trafficking-commercial-b and https://obamawhitehouse.archives.gov/the-press-office/2014/02/11/fact-sheet-national-strategy-combating-wildlife-trafficking-commercial-b for the US regulatory conditions currently governing trade in ivory, which may also apply to availability of samples). Software used in this study is available on GitHub: EBhybrids, https://github.com/stephenslab/EBhybrids; familial matching, https://github.com/cwolock/elephant_fam_match; SCAT, https://github.com/stephens999/scat; VORONOI, https://github.com/stephens999/voronoi; ivory, analysis, pipeline, https://github.com/mkkuhner/ivory_pipeline.

References

  1. Thouless, C. R. et al. African Elephant Status Report 2016: An Update from the African Elephant Database (IUCN, 2016).

  2. Maisels, F. et al. Devastating decline of forest elephants in Central Africa. PLoS ONE 8, e59469 (2013).

  3. Nishihara, T. Demand for forest elephant ivory in Japan. Pachyderm 52, 55–65 (2012).

    Google Scholar 

  4. Underwood, F. M., Burn, R. W. & Milliken, T. Dissecting the illegal ivory trade: an analysis of ivory seizures data. PLoS ONE 8, e76539 (2013).

    Article  CAS  Google Scholar 

  5. Wasser, S. K. et al. Genetic assignment of large seizures of elephant ivory reveals Africa’s major poaching hotspots. Science 349, 84–87 (2015).

    Article  CAS  Google Scholar 

  6. Wasser, S. K. et al. Combating transnational organized crime by linking multiple large ivory seizures to the same dealer. Sci. Adv. 4, eaat0625 (2018).

    Article  CAS  Google Scholar 

  7. Wasser, S. K. & Gobush, K. S. Conservation: monitoring elephant poaching to prevent a population crash. Curr. Biol. 29, R623–R646 (2019).

    Article  Google Scholar 

  8. Gershaw, C. J., Schweighardt, A. J., Rourke, L. C. & Wallaces, M. M. Forensic utilization of familial searches in DNA databases. Forensic Sci. Int. Genet. 5, 16–20 (2011).

    Article  CAS  Google Scholar 

  9. Fung, W. K. et al. Testing for kinship in a subdivided population. Forensic Sci. Int. 135, 105–109 (2003).

    Article  Google Scholar 

  10. Ward, J. H. Hierarchical grouping to optimize an objective function. J. Am. Stat. Assoc. 58, 236–244 (1963).

    Article  Google Scholar 

  11. Hanneman, R. A. & Riddle, M. Introduction to Social Network Methods (Univ. California Press, 2005).

  12. Cerling, T. E. et al. Radiocarbon dating of seized ivory confirms rapid decline in African elephant populations and provides insight into illegal trade. Proc. Natl Acad. Sci. USA 113, 13330–13335 (2016).

    Article  CAS  Google Scholar 

  13. Schlossberg, S., Chase, M. J., Gobush, K. S., Wasser, S. K. & Lindsay, K. State–space models reveal a continuing elephant poaching problem in most of Africa. Sci. Rep. 10, 10166 (2020).

  14. Blondel, V. D., Guilluame, J.-L., Lambiotte, R. & Lefebvre, E. Fast unfolding of communities in large networks. J. Stat. Mech. Theory Exp. 2008, P10008 (2008).

  15. Costa, J. Social Network Analysis Applied to Illegal Wildlife Trade Between East Africa and South East Asia (Basel Institute on Governance, 2021); https://baselgovernance.org/publications/SNA_IWT

  16. Combatting Wildlife Crime and the Illicit Exploitation of Natural Resources in the Democratic Republic of Congo (UNODC, 2021); https://www.unodc.org/unodc/en/frontpage/2021/April/combating-wildlife-crime-and-the-illicit-exploitation-of-natural-resources-in-the-democratic-republic-of-congo.html

  17. Kahumbu, P., Halliday, A. & Morrison, M. Crimes Against Wildlife and the Environment: Kenya’s Legal Response to Wildlife, Forestry and Fisheries Crime (Wildlife Direct, 2021); https://wildlifedirect.org/wp-content/uploads/2021/03/WildlifeDirect_Eyes-in-the-Courtroom_2018-2019.pdf

  18. Kahumbu, P., Karani, J. & Muriu, E. On the Right Path? An Analysis of Kenya’s Law Enforcement Response to Wildlife Crime (Wildlife Direct, 2018); https://wildlifedirect.org/wp-content/uploads/2018/08/Eyes-in-the-Courtroom-Report-2016-2017.small_.pdf

  19. Morris, C. The ‘Enterprise,’ the Burundi Stockpile, and other Ivory Behind the Extradition (International Policy Digest, 2021); https://intpolicydigest.org/the-enterprise-the-burundi-stockpile-and-other-ivory-behind-the-extradition/

  20. Out of Africa (Environmental Investigation Agency, 2020); https://reports.eia-international.org/out-of-africa/

  21. Forestry Crime: Targeting the Most Lucrative of Environmental Crimes (INTERPOL, 2020); https://www.interpol.int/News-and-Events/News/2020/Forestry-crime-targeting-the-most-lucrative-of-environmental-crimes

  22. The Kenyan connection: do dope-smugglers also peddle ivory. The Economist (9 February 2017); https://www.economist.com/middle-east-and-africa/2017/02/09/do-dope-smugglers-also-peddle-ivory

  23. Mailand, C. & Wasser, S. K. Isolation of DNA from small amounts of elephant ivory. Nat. Protoc. 2, 2228–2232 (2007).

    Article  CAS  Google Scholar 

  24. Winters, M. et al. Isolation of DNA from small amounts of elephant ivory: sampling the cementum with total demineralization extraction. Forensic Sci. Int. 288, 131–139 (2018).

    Article  CAS  Google Scholar 

  25. Nyakaana, S. & Arctander, P. Population genetic structure of the African elephant in Uganda based on variation at mitochondrial and nuclear loci: evidence for male‐biased gene flow. Mol. Ecol. 8, 1105–1115 (1999).

    Article  CAS  Google Scholar 

  26. Comstock, K. E., Wasser, S. K. & Ostrander, E. A. Polymorphic microsatellite DNA loci identified in the African elephant (Loxodona africana). Mol. Ecol. 9, 993–1011 (2000).

    Article  Google Scholar 

  27. Comstock, K. E. et al. Patterns of molecular genetic variation among African elephant populations. Mol. Ecol. 11, 2489–2498 (2002).

    Article  CAS  Google Scholar 

  28. Mondol, S. et al. New evidence for hybrid zones of forest and savanna elephants in Central and West Africa. Mol. Ecol. 24, 6134–6147 (2015).

    Article  CAS  Google Scholar 

  29. Wasser, S. K. et al. Assigning African elephant DNA to geographic region of origin: applications to the ivory trade. Proc. Natl Acad. Sci. USA 101, 14847–14852 (2004).

    Article  CAS  Google Scholar 

  30. Wasser, S. K. et al. Using DNA to track the origin of the largest ivory seizure since the 1989 trade ban. Proc. Natl Acad. Sci. USA 104, 4228–4233 (2007).

    Article  CAS  Google Scholar 

  31. Swofford, D. L. PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods) v.4 (Sinauer Associates, 2003).

  32. Saccone, C., Pesole, G. & Sbisá, E. The main regulatory region of mammalian mitochondrial DNA: structure–function model and evolutionary pattern. J. Mol. Evol. 33, 83–91 (1991).

    Article  CAS  Google Scholar 

  33. Katoh, K., Rozewicki, J. & Yamada, K. D. MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Brief Bioinform. 20, 1160–1166 (2019).

  34. Kalinowski, S. T., Taper, M. L. & Marshall, T. C. Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Mol. Ecol. 16, 1099–1106 (2007).

    Article  Google Scholar 

  35. Kluyver, T. et al. in Positioning and Power in Academic Publishing: Players, Agents and Agendas (eds Loizides, L. & Birgit Schmidt, B.) 87–90 (IOS Press, 2016).

  36. Hagberg, A., Schult, D. & Swart, P. J. Exploring network structure, dynamics, and function using NetworkX. In Proc. 7th Python in Science Conference (eds Varoquaux, G. et al.) 11–15 (SciPy, 2008).

  37. Almende, B. V., Thieurmel, B. & Robert, T. visNetwork: network visualization using ‘vis.js’ library. R version 2.0.9 https://CRAN.R-project.org/package=visNetwork (2019).

  38. Chang, W., Cheng, J., Allaire, J., Xie, Y. & McPherson, J. shiny: web application framework for R. R version 1.4.0 https://CRAN.R-project.org/package=shiny (2019).

  39. Butts, C. network: Classes for relational data. R version 1.16.1 https://CRAN.R-project.org/package=network (2019).

  40. Maechler, M., Rousseeuw, P., Struyf, A., Hubert, M. & Hornik, K. Cluster: cluster analysis basics and extensions. R version 2.1.2 https://CRAN.R-project.org/package=cluster (2021).

  41. Coombs, K. R. ClassDiscovery: classes and methods for “class discovery” with microarrays or proteomics. R version 3.3.13 https://CRAN.R-project.org/package=ClassDiscovery (2020).

  42. Rousseeuw, P. J. Silhouettes: a graphical aid to the interpretation and validation of cluster analysis. J. Comp. Appl. Math. 20, 53–65 (1987).

Download references

Acknowledgements

This works was supported by the Paul and Yaffe Maritz Family Foundation, Wildlife Conservation Network, Elephant Crisis Fund, UN Development Program, the Paul G. Allen Family Foundation, the Woodtiger Fund, the Bureau of International Narcotics and Law Enforcement Affairs of the US Department of State, US Department of Homeland Security, HSI, the World Bank, UN Office on Drugs and Crime, the National Institute of Justice (grant no. 2020-DQ-BX-0022) and National Institutes of Health (grant no. GM075091). The opinions, findings, conclusions and recommendations expressed in this paper are those of the authors and do not necessarily reflect those of the agencies or donors that funded this work. E. Thompson, J. Felsenstein and M. Taper offered statistical advice. M. Winters, R. Booth and E. Reese provided lab assistance. K. Wolfram provided logistical support. Eco Activists for Governance and Law Enforcement (EAGLE), Hong Kong AFCD, HSI-Singapore, HSI-Vietnam, INTERPOL, Kenya Wildlife Service, Mozambique National Administration of Protected Areas, Singapore NPARKS, Uganda Wildlife Authority and Uganda Revenue Authority provided sampling assistance. Environmental Investigation Agency-UK and Maisha Group Ltd contributed physical evidence. The following governments agreed to provide samples from their ivory seizures: Angola, Cote d’Ivoire, Hong Kong, Kenya, Malawi, Malaysia, Mozambique, Philippines, Singapore, Sri Lanka, South Sudan, Taiwan, Thailand, Togo, Uganda, United Arab Emirates and Vietnam.

Author information

Authors and Affiliations

  1. Center for Environmental Forensic Science, University of Washington, Seattle, WA, USA

    Samuel K. Wasser, Mary K. Kuhner, Yves Hoareau, Zofia A. Kaliszewska, Eunjin Jeon & Kin-Lan Han

  2. Department of Biostatistics, University of Washington, Seattle, WA, USA

    Charles J. Wolock & Bruce S. Weir

  3. US Department of Homeland Security, Homeland Security Investigations, Washington, DC, USA

    John E. Brown III

  4. SeeJ-Africa, Nairobi, Kenya

    Chris Morris

  5. Geospatial Data Sciences, University of Michigan School for Environment and Sustainability, Ann Arbor, MI, USA

    Ryan J. Horwitz

  6. Center for Wildlife Forensics, National Parks Board, Singapore, Singapore

    Anna Wong & Charlene J. Fernandez

  7. Forensic and Genetics Laboratory, Kenya Wildlife Service, Nairobi, Kenya

    Moses Y. Otiende

Authors
  1. Samuel K. Wasser
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Charles J. Wolock
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mary K. Kuhner
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. John E. Brown III
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Chris Morris
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Ryan J. Horwitz
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Anna Wong
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Charlene J. Fernandez
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Moses Y. Otiende
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Yves Hoareau
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Zofia A. Kaliszewska
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Eunjin Jeon
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Kin-Lan Han
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Bruce S. Weir
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

The idea for the study was conceived by S.K.W. Sampling was conducted by S.K.W., J.E.B., A.W., C.J.F. and M.Y.O. Laboratory analyses were conducted by Y.H., Z.A.K., E.J. and K.H. Familial searches and analyses were conducted by C.J.W., M.K.K. and B.S.W. Network analyses were conducted by R.H. and M.K.K. Physical evidence was compiled by J.E.B., C.M. and S.K.W. Manuscript preparation was by S.K.W., M.K.K., C.J.W., J.E.B., C.M. and R.H. Manuscript edits were by S.K.W., C.J.W., J.E.B., C.M., R.H., M.K.K. and B.S.W.

Corresponding author

Correspondence to Samuel K. Wasser.

Ethics declarations

Competing interests

The authors declare no competing interests.

Peer review

Peer review information

Nature Human Behaviour thanks the anonymous reviewers for their contribution to the peer review of this work. Peer reviewer reports are available.

Additional information

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

Extended data

Extended Data Fig. 1 Genetic matches between tusks found in separate ivory seizures.

Format is the same as in Fig. 3a. Seizure number key: 1 = SGP, 06-02, 6.5t; 2 = HKG, 05-06, 3.9t; 3 = HKG, 07-06, 2.6t; 4 = TWN, 07-06, 1.2t; 5 = TWN, 07-06, 3.0t; 6 = SGP, 03-07, 0.5t; 7 = PHL, 06-09, 4.9t; 8 = VNM, 04-10, 2.2t; 9 = KEN, 08-10, 1.5t; 10 = THA, 01-11, 0.33t; 11 = KEN, 05-11, 1.3t; 12 = MYS, 09-11, 1.1t; 13 = KEN, 12-11, 1.5t; 14 = LKA, 05-12, 1.5t; 15 = UGA, 09-12, Xt,;16 = HKG, 10-12, 1.9tA; 17 = HKG, 10-12, 1.9tB; 18 = MYS, 12-12, 6.0t; 19 = HKG, 01-13, 1.3t; 20 = KEN, 01-13, 3.8t; 21 = ARE, 05-13, 1.5t; 22 = MWI, 05-13, 2.6t; 23 = KEN, 06-13, 1.5t; 24 = HKG, 07-13, 2.0t; 25 = KEN, 07-13, 3.3t; 26 = HKG, 08-13, 2.2t; 27 = TGO, 08-13, 0.7t; 28 = KEN, 10-13, 2.0t; 29 = KEN, 10-13, 2.9t; 30 = UGA, 10-13, 2.9t; 31 = UGA, 12-13, 1.4t; 32 = TGO, 01-14, 3.9t; 33 = SGP, 03-14, 1.0t; 34 = UGA, 05-14, 1.8t; 35 = KEN, 06-14, 2.2t; 36 = UGA, 07-14, 0.6t; 37 = MOZ, 05-15, 1.2t; 38 = SGP, 05-15, 4.6t; 39 = SSD, 06-16, 0.5t; 40 = MYS, 07-16, 0.89t; 41 = KEN, 12-16, 1.0t; 42 = MYS, 01-17, 0.85t; 43 = UGA, 02-17, 1.3t; 44 = HKG, 07-17, 7.2t; 45 = CIV, 01–18, 0.5t; 46 = SGP, 03-18, 3.3t; 47 = AGO, 06-18, 1.8t; 48 = UGA, 01-19, 3.3t; 49 = SGP, 07-19, 8.8t. ISO Key: AGO = Angola, ARE = United Arab Emirates, CIV = Cote d’Ivoire, HKG = Hong Kong, KEN = Kenya, LKA = Sri Lanka, MOZ = Mozambique, MWI = Malawi, MYS = Malaysia, PHL = Philippines, SGP = Singapore, SSD = South Sudan, TGO = Togo, THA = Thailand, TWN = Taiwan, UGA = Uganda, VNM = Vietnam.

Extended Data Fig. 2 Physical-evidence matches between tusks found in separate ivory seizures.

Format is the same as in Fig. 3b.

Supplementary information

Supplementary Information

Supplementary Tables 1–7 and description of extraction methods.

Reporting Summary.

Peer Review Information.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Wasser, S.K., Wolock, C.J., Kuhner, M.K. et al. Elephant genotypes reveal the size and connectivity of transnational ivory traffickers. Nat Hum Behav 6, 371–382 (2022). https://doi.org/10.1038/s41562-021-01267-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41562-021-01267-6

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

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