Cooperation and individuality among man-eating lions

Edited by Kristen Hawkes, University of Utah, Salt Lake City, UT, and approved September 25, 2009
November 10, 2009
106 (45) 19040-19043

Abstract

Cooperation is the cornerstone of lion social behavior. In a notorious case, a coalition of two adult male lions from Tsavo, southern Kenya, cooperatively killed dozens of railway workers in 1898. The “man-eaters of Tsavo” have since become the subject of numerous popular accounts, including three Hollywood films. Yet the full extent of the lions' man-eating behavior is unknown; estimates range widely from 28 to 135 victims. Here we use stable isotope ratios to quantify increasing dietary specialization on novel prey during a time of food limitation. For one lion, the δ13C and δ15N values of bone collagen and hair keratin (which reflect dietary inputs over years and months, respectively) reveal isotopic changes that are consistent with a progressive dietary specialization on humans. These findings not only support the hypothesis that prey scarcity drives individual dietary specialization, but also demonstrate that sustained dietary individuality can exist within a cooperative framework. The intensity of human predation (up to 30% reliance during the final months of 1898) is also associated with severe craniodental infirmities, which may have further promoted the inclusion of unconventional prey under perturbed environmental conditions.

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Acknowledgments.

We thank A. K. Behrensmeyer, E. E. Butler, C. E. Chow, C. T. Darimont, J. A. Estes, L. Gahegan, P. Hluzova, J. B. Hopkins, S. D. Newsome, J. D. Phelps, J.W. Ridges, W. Stanley, R. H. Tuttle, E. R. Vogel, P. V. Wheatley, and C. C. Wilmers for helpful comments and discussions. We thank the Duckworth Laboratory, the Field Museum of Natural History, and the Smithsonian National Museum of Natural History for access to unpublished field reports. Modern samples were imported under CITES import no. US-012 (PRT 701716). This study was approved by the Chancellor's Animal Research Committee of University of California (UC)-Santa Cruz (no. Domin0806) and approved as exempt by the Institutional Review Board of UC-Santa Cruz (no. HS0801187). This study was funded by the Earthwatch Institute, the David and Lucile Packard Foundation, and a grant from the UC-Santa Cruz Committee on Research.

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References

1
DI Bolnick, et al., The ecology of individuals: Incidence and implications of individual specialization. Am Nat 161, 1–28 (2002).
2
DI Bolnick, R Svanbäck, MS Araújo, L Persson, Comparative support for the niche variation hypothesis that more generalized populations also are more heterogeneous. Proc Natl Acad Sci USA 104, 10075–10079 (2007).
3
CT Darimont, PC Paquet, TE Reimchen, Landscape heterogeneity and marine subsidy generate extensive intrapopulation niche diversity in a large terrestrial vertebrate. J Anim Ecol 78, 126–133 (2009).
4
GB Schaller The Serengeti Lion: A Study of Predator-Prey Relations (Univ of Chicago Press, Chicago, 1972).
5
C Packer, D Scheel, AE Pusey, Why lions form groups: Food is not enough. Am Nat 136, 1–19 (1990).
6
C Packer, et al., Ecological change, group territoriality, and population dynamics in Serengeti lions. Science 307, 390–393 (2005).
7
PE Stander, Cooperative hunting in lions: The role of the individual. Behav Ecol Sociobiol 29, 445–454 (1992).
8
R Heinsohn, C Packer, Complex cooperative strategies in group-territorial African lions. Science 269, 1260–1262 (1995).
9
C Packer, L Ruttan, The evolution of cooperative hunting. Am Nat 132, 159–198 (1988).
10
JA Estes, ML Riedman, MM Staedler, MT Tinker, BE Lyon, Individual variation in prey selection by sea otters: Patterns, causes and implications. J Anim Ecol 72, 144–155 (2003).
11
C Packer, D Ikanda, B Kissui, H Kushnir, Lion attacks on humans in Tanzania. Nature 436, 927–928 (2005).
12
JC Kerbis Peterhans, TP Gnoske, The science of ‘man-eating’ among lions Panthera leo with a reconstruction of the natural history of the ‘man-eaters of Tsavo’. J East Afr Nat Hist 90, 1–40 (2001).
13
EH Merritt, A History of the Taita of Kenya to 1900. (Department of History, Indiana University, Bloomington, IN, PhD dissertation. (1975).
14
BD Patterson The Lions of Tsavo: Exploring the Legacy of Africa's Notorious Man-Eaters (McGraw-Hill, New York, 2004).
15
JH Patterson The Man-Eating Lions of Tsavo (Field Museum of Natural History, Chicago, 1925).
16
JH Patterson The Man-Eaters of Tsavo and Other East African Adventures (Macmillan, London, 1907).
17
EJ Neiburger, BD Patterson, A forensic dental determination of serial killings by three African lions. Gen Dent 50, 40–42 (2002).
18
BD Patterson, EJ Neiburger, SM Kasiki, Tooth breakage and dental disease as causes of carnivore-human conflicts. J Mammal 84, 190–196 (2003).
19
SD Newsome, C Martinez del Rio, S Bearhop, DL Phillips, A niche for isotopic ecology. Front Ecol Environ 5, 429–436 (2007).
20
JW Moore, BX Semmens, Incorporating uncertainty and prior information into stable isotope mixing models. Ecol Lett 11, 470–480 (2008).
21
LL Tieszen, TW Boutton, KG Tesdahl, NA Slade, Fractionation and turnover of stable carbon isotopes in animal tissues: Implications for δ13C analysis of diet. Oecologia 57, 32–37 (1983).
22
LSB Leakey The East African Archaeological Expedition: Season 1928–1929. Report for September, October and November (National Anthropological Archives, Smithsonian Institution, Washington, DC, Unpublished report. (1929).
23
SH Ambrose, Stable carbon and nitrogen isotope analysis of human and animal diet in Africa. J Hum Evol 15, 707–731 (1986).
24
SH Ambrose, MJ Deniro, Reconstruction of African human diet using bone-collagen carbon and nitrogen isotope ratios. Nature 319, 321–324 (1986).
25
PG Bostock The Peoples of Kenya: The Taita (Macmillan, London, 1950).
26
CW Hobley, Upon a visit to Tsavo and the Taita Highlands. Geogr J 5, 545–561 (1895).
27
SH Ambrose, L Norr Prehistoric Human Bone: Archaeology at the Molecular Level, eds JB Lambert, G Grupe (Springer, Berlin), pp. 1–37 (1993).
28
SH Ambrose, MJ Deniro, The isotopic ecology of East African mammals. Oecologia 69, 395–406 (1986).
29
J Corbett Man-Eaters of Kumaon (H. Milford, London, 1944).
30
D Livingstone Missionary Travels and Researches in South Africa (Harper and Brothers, New York, 1868).
31
B Green, J Anderson, T Whateley, Water and sodium turnover and estimated food consumption in free-living lions (Panthera leo) and spotted hyaenas (Crocuta crocuta). J Mammal 65, 593–599 (1984).
32
RW Kays, BD Patterson, Mane variation in African lions and its social correlates. Can J Zool 80, 471–478 (2002).
33
C Packer, AE Pusey, LE Eberly, Egalitarianism in female African lions. Science 293, 690–693 (2001).
34
M Eppinger, et al., Who ate whom? Adaptive Helicobacter genomic changes that accompanied a host jump from early humans to large felines. PLoS Genet 2, 1097–1110 (2006).
35
E Kitson, A study of the negro skull with special reference to the crania from Kenya Colony. Biometrika 23, 271–314 (1931).
36
GB Nardoto, PB Godoy, ESB Ferraz, JPHB Ometto, LA Martinelli, Stable carbon and nitrogen isotopic fractionation between diet and swine tissues. Sci Agric 63, 579–582 (2006).
37
JD Roth, KA Hobson, Stable carbon and nitrogen isotopic fractionation between diet and tissue of captive red fox: Implications for dietary reconstruction. Can J Zool 78, 848–852 (2000).
38
M Leuenberger, U Siegenthaler, C Langway, Carbon isotope composition of atmospheric CO2 during the last ice age from an Antarctic ice core. Nature 357, 488–490 (1992).
39
C Hollis, Notes on the history and customs of the people of Taveta, East Africa. J Roy Afr Soc 1, 98–125 (1901).

Information & Authors

Information

Published in

Go to Proceedings of the National Academy of Sciences
Proceedings of the National Academy of Sciences
Vol. 106 | No. 45
November 10, 2009
PubMed: 19884504

Classifications

Submission history

Received: May 13, 2009
Published online: November 10, 2009
Published in issue: November 10, 2009

Keywords

  1. individual dietary specialization
  2. Panthera leo
  3. Taita
  4. Tsavo

Acknowledgments

We thank A. K. Behrensmeyer, E. E. Butler, C. E. Chow, C. T. Darimont, J. A. Estes, L. Gahegan, P. Hluzova, J. B. Hopkins, S. D. Newsome, J. D. Phelps, J.W. Ridges, W. Stanley, R. H. Tuttle, E. R. Vogel, P. V. Wheatley, and C. C. Wilmers for helpful comments and discussions. We thank the Duckworth Laboratory, the Field Museum of Natural History, and the Smithsonian National Museum of Natural History for access to unpublished field reports. Modern samples were imported under CITES import no. US-012 (PRT 701716). This study was approved by the Chancellor's Animal Research Committee of University of California (UC)-Santa Cruz (no. Domin0806) and approved as exempt by the Institutional Review Board of UC-Santa Cruz (no. HS0801187). This study was funded by the Earthwatch Institute, the David and Lucile Packard Foundation, and a grant from the UC-Santa Cruz Committee on Research.

Notes

This article is a PNAS Direct Submission.
This article contains supporting information online at www.pnas.org/cgi/content/full/0905309106/DCSupplemental.

Authors

Affiliations

Justin D. Yeakel1 [email protected]
Department of Ecology and Evolutionary Biology, University of California, Santa Cruz, 1156 High Street, Santa Cruz, CA 95064;
Bruce D. Patterson
Department of Zoology, Field Museum of Natural History, 1400 South Lake Shore Drive, Chicago, IL 60605;
Kena Fox-Dobbs
Department of Geology, University of Puget Sound, 1500 North Warner Street, CMB 1048, Tacoma, WA 98416-1048;
Mercedes M. Okumura
Leverhulme Centre for Human Evolutionary Studies, University of Cambridge, Fitzwilliam Street, Cambridge CB2 1QH, United Kingdom;
Thure E. Cerling
Department of Geology and Geophysics, University of Utah, 135 South 1460 E, Salt Lake City, UT 84112;
Jonathan W. Moore
Department of Ecology and Evolutionary Biology, University of California, Santa Cruz, 100 Shaffer Road, Santa Cruz, CA 95060; and
Paul L. Koch
Departments of gEarth and Planetary Sciences and
Nathaniel J. Dominy1 [email protected]
Department of Ecology and Evolutionary Biology, University of California, Santa Cruz, 1156 High Street, Santa Cruz, CA 95064;
Anthropology, University of California, Santa Cruz, 1156 High Street, Santa Cruz, CA 95064

Notes

1
To whom correspondence may be addressed. E-mail: [email protected] or [email protected]
Author contributions: J.D.Y., B.D.P., P.L.K., and N.J.D. designed research; J.D.Y., B.D.P., and N.J.D. performed research; K.F.-D., M.M.O., and T.E.C. contributed new reagents/analytic tools; J.D.Y., B.D.P., K.F.-D., J.W.M., P.L.K., and N.J.D. analyzed data; and J.D.Y., B.D.P., P.L.K., and N.J.D. wrote the paper.

Competing Interests

The authors declare no conflict of interest.

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    Cooperation and individuality among man-eating lions
    Proceedings of the National Academy of Sciences
    • Vol. 106
    • No. 45
    • pp. 18875-19204

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