Abstract
The honey badger is a widespread, but understudied African carnivore, with high potential as a bone accumulator in cave and fossil deposits. This study serves as the first investigation into the taphonomic modifications of this species when feeding on small to medium-sized prey. Domestic rabbit (Oryctolagus cunniculus) carcasses where fed experimentally to a breeding pair of captive honey badgers housed at the Johannesburg Zoo. Bones from the feeding refuse and the carnivore scats were analysed for anatomical composition, fragmentation patterns, tooth marks and digestion. The results were compared with feeding studies with various small carnivores on leporid prey. Honey badgers preferentially opened their prey at the belly and focussed their feeding on nutritionally high-yield soft parts, often discarding low-yield parts like distal appendages, crania and the skins. Bones from the refuse assemblage were often complete and unmodified but stripped of flesh. Bones from the scat assemblage displayed very high fragmentation, light digestive modification and high numbers of tooth marked bones. This latter character was particularly diagnostic for the honey badger. This study investigates a carnivore that has received little interest and shows the high potential of this carnivore to act as a bone accumulator. Further taphonomic research into this species will greatly enhance our understanding of this species and its activity in the fossil record.
Similar content being viewed by others
References
Adams JW, Herries AIR, Kuykendall KL, Conroy GC (2007) Taphonomy of a South African cave: geological and hydrological influences on the GD 1 fossil assemblage at Gondolin, a Plio-Pleistocene paleocave system in the Northwest Province, South Africa. Quaternary Sci Rev 26:2526–2543
Álvarez MC, Kaufmann CA, Massigoge A, Gutiérrez MA, Rafuse DJ, Scheifler NA, González AE (2012) Bone modification and destruction patterns of leporid carcasses by Geoffroy’s cat (Leopardus geoffroyi): an experimental study. Quatern Int 278:71–80
Andrés M, Gidna AO, Yravedra J, Domínguez-Rodrigo M (2012) A study of dimensional differences of tooth marks (pits and scores) on bones modified by small and large carnivores. Archaeol Anthropol Sci 4(3):209–219
Andrews P (1990) Owls, caves and fossils. Natural History Museum Publications, London
Andrews P, Evans EMN (1983) Small mammal bone accumulations produced by mammalian carnivores. Paleobiology 9(3):289–307
Argenti P, Kotsakis T (2009) The fossil remains of Soricidae and Leporidae (Mammalia) in the lower Pleistocene of Pietrafitta (Perugia, Central Italy). Boll Soc Paleontol Ital 48(1):59–62
Armstrong A (2016) Eagles, owls, and coyotes (oh my!): taphonomic analysis of rabbits and guinea pigs fed to captive raptors and coyotes. J Archaeol Sci: Reports 5:135–155. https://doi.org/10.1016/j.jasrep.2015.10.039
Avery G, Cruz-Uribe K, Goldberg P et al (1997) The 1992–1993 excavations at the Die Kelders Middle and Later Stone Age Cave site, South Africa. J Field Archaeol 24(3):263–291
Avery G, Halkett D, Orton J, Steele T, Tusenius M, Klein R (2008) The Ysterfontein 1 Middle Stone Age rock shelter and the evolution of coastal foraging. S Afr Archaeol Soc Goodwin Series 10:66–89
Begg CM, Begg KS, Du Toit JT, Mills MGL (2003) Sexual and seasonal variation in the diet and foraging behaviour of a sexually dimorphic carnivore, the honey badger (Mellivora capensis). J Zoo, London 260:301–316
Begg CM, Begg KS, Du Toit JT, Mills MGL (2005) Spatial organisation of the honey badger Mellivora capensis in the southern Kalahari: home-range size and movement patterns. J Zool (Lond) 265:23–35
Berger LR, Clarke RJ (1995) Eagle involvement in accumulation of the Taung child faunas. J Hum Evol 26:275–299
Binford LR (1981) Bones: ancient men and modern myths. Academic Press, New York
Bountalis AC, Kuhn BF (2014) Cave usage by multiple taphonomic agents: issues towards interpreting the fossil bearing cave deposits in South Africa. Am J Zool Res 2(4):55–61
Campmas É, Beauval C (2008) Consommation osseuse des carnivores: résultats de l’étude de l’exploitation de carcasses de bœufs (Bos taurus) par des loups captifs. Ann Paléontol 94(3):167–186 Available at: http://linkinghub.elsevier.com/retrieve/pii/S0753396908000396
Cohen BF (2013) Actualistic investigation of bone modification on leporids by caracal (Caracal caracal) and honey badger (Mellivora capensis); An insight to the taphonomy of Cooper’s Cave, South Africa. MSc thesis, University of the Witwatersrand, Johannesburg.
Cohen BF, Kibii JM (2015) Experimental study of bone modification by captive caracal (Caracal caracal); a model for fossil assemblage analysis. J Archaeol Sci 62:92–104 Available at: http://linkinghub.elsevier.com/retrieve/pii/S0305440315002307
Delaney-Rivera C, Plummer TW, Hodgson JA, Forrest F, Hertel F, Oliver JS (2009) Pits and pitfalls: taxonomic variability and patterning in tooth mark dimensions. J Archaeol Sci 36(11):2597–2608 Available at: http://linkinghub.elsevier.com/retrieve/pii/S0305440309002726
Dodson P, Wexlar D (1979) Taphonomic investigations of owl pellets. Paleobiology 5(3):275–284
Domínguez-Rodrigo M (1999) Flesh availability and bone modifications in carcasses consumed by lions: palaeoecological relevance in hominid foraging patterns. Palaeogeogr Palaeocl 149:373–388
Domı́nguez-Rodrigo M, Martínez-Navarro B (2012) Taphonomic analysis of the early Pleistocene (2.4 Ma) faunal assemblage from A.L. 894 (Hadar Ethiopia). J Hum Evol 62(3):315–327
Esteban-Nadal M, Cáceres I, Fosse P (2010) Characterization of a current coprogenic sample originated by Canis lupus as a tool for identifying a taphonomic agent. J Archaeol Sci 37(12):2959–2970 Available at: http://linkinghub.elsevier.com/retrieve/pii/S030544031000230X
Fa JE, Stewart JR, Lloveras L, Vargas JM (2013) Rabbits and hominin survival in Iberia. J Hum Evol 64(4):233–241. https://doi.org/10.1016/j.jhevol.2013.01.002
Fernández-Jalvo Y, Andrews P (1992) Small mammal taphonomy of Gran Dolina, Atapuerca (Burgos), Spain. J Archaeol Sci 19:407–428
Fostowicz-Frelik Ł, Gasparik M (2006) The taxonomic status of leporid remains from Ördöglyuk Cave, Solymár (Hungary). Acta Zool Cracov Ser A: Vertebrata 49(1):151–161
Geraads D (2006) The Late Pliocene locality of Ah1 a1 Oughlam, Morocco: vertebrate fauna and interpretation. T Roy Soc S Afr 61(2):97–101. https://doi.org/10.1080/00359190609519958
Geraads D, Alemseged Z, Reed D, Wynn J, Roman DC (2004) The Pleistocene fauna (other than primates) from Asbole, lower Awash Valley, Ethiopia, and its environmental and biochronological implications. Geobios 37(6):697–718 Available at: http://linkinghub.elsevier.com/retrieve/pii/S0016699504000981
Gidna A, Yravedra J, Domínguez-Rodrigo M (2013) A cautionary note on the use of captive carnivores to model wild predator behaviour: a comparison of bone modification patterns on long bones by captive and wild lions. J Archaeol Sci 40:1903–1910
Gidna A, Domínguez-Rodrigo M, Pickering TR (2015) Patterns of bovid long limb bone modification created by wild and captive leopards and their relevance to the elaboration of referential frameworks for paleoanthropology. J Archaeol Sci: Rep 2:302–309
Gommery D, Thackeray JF, Potze S, Braga J (2008) The first recorded occurrence of honey badger of the genus Mellivora (Carnivora: Mustelidae) at Kromdraai B. S Afr Ann Transv Mus 45:145–148
Haile-Selassie Y, Hlusko LJ, Howell FC (2004) A new species of Plesiogulo (Mustelidae: Carnivora) from the late Miocene of Africa. Pal Afr 40(December):85–88
Haynes G (1980) Evidence of carnivore gnawing on Pleistocene and recent mammalian bones evidence of carnivore gnawing on Pleistocene and recent mammalian bones. Paleobiology 6(3):341–351
Hendey QB (1974) The Late Cenozoic carnivora of the South-western Cape Province. Ann South Afr Mus 63:1–369
Hendey QB (1978) Late Tersiary Mustelidae from Langebaanweg, South Africa. Ann S Afr Mus 76(10):329–357
Hewson R (1984) Scavenging and predation upon sheep and lambs in West Scotland. J Appl Ecol 21(3):843–868
Hockett BS (1994) A descriptive reanalysis of the leporid bones from Hogup Cave. Utah J Calif Gt Basin Anthropol 16(1):106–117
Hockett BS, Haws JA (2002) Taphonomic and methodological perspectives of leporid hunting during the upper Paleolithic of the western Mediterranean Basin. J Archaeol Meth Th 9(3):269–302
James EC, Thompson JC (2015) On bad terns: problems and solutions within zooarchaeological bone surface modification studies. Environ Archaeol 20(1):89–103. https://doi.org/10.1179/1749631414Y.0000000023
Kingdon J (1977) East African mammals, an Atlas of evolution in Africa, volume 3A. Academic Press, London
Klein RG, Cruz-Uribe K, Halkett D, Hart T, Parkington JE (1999) Paleoenvironmental and human behavioral implications of the Boegoeberg 1 Late Pleistocene Hyena Den, Northern Cape Province. S Afr Q Res 52(3):393–403 Available at: http://linkinghub.elsevier.com/retrieve/pii/S0033589499920689
Klein RG, Avery G, Cruz-Uribe K, Steele TE (2007) The mammalian fauna associated with an archaic hominin skullcap and later Acheulean artifacts at Elandsfontein, Western Cape Province, South Africa. J Hum Evol 52(2):164–186. https://doi.org/10.1016/j.jhevol.2006.08.006
Kovarovic K, Andrews P, Aiello L (2002) The palaeoecology of the Upper Ndolanya beds at Laetoli, Tanzania. J Hum Evol 43(3):395–418
Krajcarz M, Krajcarz MT (2012) The red fox (Vulpes vulpes) as an accumulator of bones in cave-like environments. Int J Osteoarchaeol 24(4):459–475
Kruuk H, Mills MGL (1983) Notes on food and foraging of the honey badger (Mellivora capensis) in the Kalahari Gemsbok National Park. Koedoe 26:153–157
Lacruz R, Ungar P, Hancox PJ, Brink JS, Berger LR (2003) Gladysvale: fossils, strata and GIS analysis. S Afr J Sci 99:283–285
Lloveras L, Moreno-Garcia M, Nadal J (2008a) Taphonomic study of leporid remains accumulated by the Spanish imperial eagle (Aquila adalberti). Geobios 41(1):91–100. https://doi.org/10.1016/j.geobios.2006.11.009
Lloveras L, Moreno-García M, Nadal J (2008b) Taphonomic analysis of leporid remains obtained from modern Iberian lynx (Lynx pardinus) scats. J Archaeol Sci 35(1):1–13. https://doi.org/10.1016/j.jas.2007.02.005
Lloveras L, Moreno-García M, Nadal J (2009) The eagle owl (Bubo bubo) as a leporid remains accumulator: taphonomic analysis of modern rabbit remains recovered from nests of this predator. Int J Osteoarchaeol 19:573–592. https://doi.org/10.1016/j.jas.2007.02.005.
Lloveras L, Moreno-García M, Nadal J, Maroto J, Soler J, Soler N (2010) The application of actualistic studies to assess the taphonomic origin of Musterian rabbit accumulations from Arbreda Cave (North-East Iberia). Archaeofauna 19:99–119
Lloveras L, Moreno-García M, Nadal J, Zilhão J (2011) Who brought in the rabbits? Taphonomical analysis of Mousterian and Solutrean leporid accumulations from Gruta do Caldeirão (Tomar, Portugal). J Archaeol Sci 38(9):2434–2449. https://doi.org/10.1016/j.jas.2011.05.012
Lloveras L, Moreno-García M, Nadal J (2012) Assessing the variability in taphonomic studies of modern leporid remains from eagle owl (Bubo bubo) nest assemblages: the importance of age of prey. J Archaeol Sci 39(12):3754–3764. https://doi.org/10.1016/j.jas.2012.06.033
Lloveras L, Nadal J, Moreno-García M (2014) The role of the Egyptian vulture (Neophron percnopterus) as a bone accumulator in cliff rock shelters: an analysis of modern bone nest assemblages from North-Eastern Iberia. J Archaeol Sci 44:76–90. https://doi.org/10.1016/j.jas.2014.01.018
Lloveras L, Thomas R, Cosso A, Pinyol C, Nadal J (2016) When wildcats feed on rabbits: an experimental study to understand the taphonomic signature of European wildcats (Felis silvestris silvestris). Archaeol Anthropol Sci. https://doi.org/10.1007/s12520-016-0364-6
McGraw WS, Cooke C, Schultz S (2006) Primate remains from African crowned eagle (Stephanoaetus coronatus) nest in Ivory Coast’s Tai forest: implications for primate predation and early hominid taphonomy in South Africa. Am J Phys Anthropol 131:151–165
Nakaya H (1994) Faunal change of Late Miocene Africa and Eurasia: mammalian fauna from the Namurungule formation, Samburu Hills, Northern Kenya. Afr StudMonographs, Suppl 20:1–112
Nocchi G, Sala B (1997) The fossil rabbit from Valdemino Cave (Borgio Verezzi, Savona) in the context of Western Europe Oryctolagini of quaternary. Palaeovertebrata 26(1–4):167–187
O’Regan HJ, Cohen BF, Steininger CM (2013) Mustelid and viverrid remains from the Pleistocene site of Cooper’s D, Gauteng, South Africa. Pal Afr 48(December):19–23
Pavao B, Stahl PW (1999) Structural density assays of Leporid skeletal elements with implications for taphonomic. Actual Archaeol Res J Archaeol Sci 26(1):53–66 Available at: http://linkinghub.elsevier.com/retrieve/pii/S0305440398902990
Petter G (1987) Small carnivores (Viverridae, Mustelidae, Canidae) from Laetoli. In Laetoli: a Pliocene site in Northern Tanzania: 194–234
Plug I (2004) Resource exploitation: animal use during the Middle Stone Age at Sibudu Cave, KwaZulu-Natal. S Afr J Sc 100(3–4):151–158
Pobiner, B (2007) Hominid-carnivore interactions: evidence from modern carnivore bone modification and early Pleistocene archaeofaunas (Koobi For A, Kenya; Olduvai Gorge, Tanzania). Dissertation, Rutgers University.
Pobiner B (2008) Apples and oranges again: comment on “conceptual premises in experimental design and their bearing on the use of analogy: an example from experiments on cut marks”. World Archaeol 40:466–479
Prendergast ME, Domínguez-Rodrigo M (2008) Taphonomic analyses of a hyena den and natural death assemblage near Lake Eyasi (Tanzania). J Taphonomy 6:301–335
Reynard JP, Discamps E, Badenhorst S, van Niekerk K, Henshilwood CS (2015) Subsistence strategies in the southern Cape during the Howiesons Poort: Taphonomic and zooarchaeological analyses of Klipdrift Shelter, S Afr Q Int: https://doi.org/10.1016/j.quaint.2015.07.041, 404, 2, 19.
Reynolds SC, Kibii JM (2011) Sterkfontein at 75: review of palaeoenvironments, fauna and archaeology from the hominin site of Sterkfontein (Gauteng Province, South Africa). Pal Afr 46:59–88
Rodríguez-Hidalgo A, Saladíe P, Marín J, Canals A (2013) Feeding behaviour and taphonomic characterization of non-ingested rabbit remains produced by the iberian lynx (Lynx pardinus). J Archaeol Sci 40(7):3031–3045. https://doi.org/10.1016/j.jas.2013.03.006
Rodríguez-Hidalgo A, Saladíe P, Marín J, Canals A (2015) Expansion of the referential framework for the rabbit fossil accumulations generated by Iberian lynx. Palaeogeogr Palaeocl 418:1–11. https://doi.org/10.1016/j.palaeo.2014.11.010
Rodríguez-Hidalgo A, Saladíe P, Marín J, Canals A (2016) Bird-bone modifications by Iberian lynx: a taphonomic analysis of non-ingested red-legged partridge remains. Quat Int 421:228–238. https://doi.org/10.1016/j.quaint.2015.11.078
Rosevear DR (1974) The Carnivores of West Africa, Trustees of the British Museum (Natural History) Publication no. 723, London.
de Ruiter DJ, Brophy JK, Lewis PJ, Churchill SE, Berger LR (2008) Faunal assemblage composition and paleoenvironment of Plovers Lake, a Middle Stone Age locality in Gauteng Province, South Africa. J Hum Evol 55(6):1102–1117. https://doi.org/10.1016/j.jhevol.2008.07.011
de Ruiter DJ, Pickering R, Steininger CM, Kramers JD, Hancox PJ, Churchill SE, Berger LR, Backwell L (2009) New Australopithecus robustus fossils and associated U-Pb dates from Cooper’s Cave (Gauteng, South Africa). J Hum Evol 56(5):497–513. https://doi.org/10.1016/j.jhevol.2009.01.009
Sala N, Arsuaga JL (2013) Taphonomic studies with wild brown bears (Ursus arctos) in the mountains of northern Spain. J Archaeol Sci 40:1389–1396
Sala N, Arsuaga JL (2018) Regarding beasts and humans: a review of taphonomic works with living carnivores. Quat Int 466:131–140
Schmitt DN, Juell KE (1994) Towards the identification of coyote scatological faunal accumulations in archaeological contexts. J Archaeol Sci 21:249–262
Selvaggio MM, Wilder J (2001) Identifying the involvement of multiple carnivore taxa with archaeological bone assemblages. J Archaeol Sci 28(5):465–470. https://doi.org/10.1006/jasc.2000.0557
Sikes SK (1963) A bundle of fun, pep and power—the self-confident ratel. Anim Kingdom 66:146–151
Skinner JD, Chimimba CT (2005) The mammals of the Southern African subregion, Third edn. Cambridge University Press, Cape Town
Souttou K, Manaa A, Stoetzel E, Sekour M, Hamani A, Doumandji S, Denys C (2012) Small mammal bone modifications in black- shouldered kite (Elanus caeruleus) pellets from Algeria: implications for archaeological sites. J Taphonomy 10(1):1–19
Steele TE, Klein RG (2013) The Middle and Later Stone Age faunal remains from Diepkloof Rock Shelter, Western Cape, South Africa. J Archaeol Sci 40(9):3453–3462. https://doi.org/10.1016/j.jas.2013.01.001
Tewes ME, Mock JM, Young JH (2002) Bobcat predation on quail, birds, and mesomammals. In: DeMaso SJ, Kuvlesky WP Jr, Hernandez F, Berger ME (eds) Quail V: proceedings of the fifth National Quail Symposium. Texas Parks and Wildlife Department, Austin, TX, pp 65–70
Val A, Mallye J-B (2011) Small carnivore skinning by professionals: skeletal modifications and implications for the European upper Palaeolithic. Journal of Taphonomy 9(4):221–243
Watson V (1993) Composition of the Swartkrans bone accumulations, in terms of skeletal parts and animals represented, In: Brain, C.K. ed. Swartkrans; a cave’s chronicle of early man, Pretoria: No. 8, Museum monographs: 35–73.
Werdelin L (2003) Mio-Pliocene Carnivora from Lothagam, Kenya. In: Leakey MG, Harris JD (eds) Lothagam: dawn of humanity in eastern Africa. Columbia University Press, New York, pp 261–328
Werdelin L, Lewis ME (2005) Plio-Pleistocene Carnivora of eastern Africa: species richness and turnover patterns. Zoo J Lin Soc-Lond 144:121–144
Acknowledgements
We would like to express our gratitude to all the staff of the Johannesburg Zoo, particularly Dominic Moss (Executive manager of conservation and research) and Agnes Maluleke (Carnivore curator) for their assistance with managing and coordinating this project. Thanks must go to Lorna Fuller (Senior manager for nutrition and environment) for her tireless work in sourcing rabbits. The biggest appreciation goes to the small carnivore (cat) keepers Tish and Nadia for their assistance with conducting the feedings and collecting of remains. This investigation was possible due to grants from The National Research Foundation (NRF), The Palaeontological Scientific Trust (PAST) and the Centre of Excellence (CoE) in Palaeosciences at the University of the Witwatersrand, Johannesburg.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Cohen, B.F., Kibii, J.M. Taphonomy of a novel small carnivore: experimental analysis of honey badger (Mellivora capensis) modifications on leporid prey. Archaeol Anthropol Sci 11, 2309–2327 (2019). https://doi.org/10.1007/s12520-018-0673-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12520-018-0673-z