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Primates

, Volume 59, Issue 5, pp 483–494 | Cite as

Potential self-medication using millipede secretions in red-fronted lemurs: combining anointment and ingestion for a joint action against gastrointestinal parasites?

  • Louise R. Peckre
  • Charlotte Defolie
  • Peter M. Kappeler
  • Claudia Fichtel
Original Article

Abstract

Self-anointing, referring to the behaviour of rubbing a material object or foreign substance over different parts of the body, has been observed in several vertebrate species, including primates. Several functions, such as detoxifying a rich food source, social communication and protection against ectoparasites, have been proposed to explain this behaviour. Here, we report observations of six wild red-fronted lemurs (Eulemur rufifrons) of both sexes and different age classes anointing their perianal-genital areas and tails with chewed millipedes. Several individuals also ingested millipedes after prolonged chewing. In light of the features of the observed interactions with millipedes, and the nature and potential metabolic pathways of the released chemicals, we suggest a potential self-medicative function. Specifically, we propose that anointing combined with the ingestion of millipedes’ benzoquinone secretions by red-fronted lemurs may act in a complementary fashion against gastrointestinal parasite infections, and more specifically Oxyuridae nematodes, providing both prophylactic and therapeutic effects.

Keywords

Fur-rubbing Benzoquinones Diplopods Nematodes Oxyuridae 

Notes

Acknowledgements

We thank the Malagasy Ministère de l’Environnement et des Eaux et Forêts, the Département de Biologie Animale of Antananarivo University, and the Centre National de Formation, d’Etudes et de Recherche en Environnement et Foresterie for supporting and authorising our long-term research in Kirindy. We are most grateful to the local team of the Kirindy field station, particularly to Jean-Pierre Tolojanahary, Remi and Brunot Tsiverimana for sample collection. We are very grateful to Daniel González Acosta, a PhD student in biochemistry, for his precious guidance, review and literature recommendations on the biochemical aspects of this work, and his contribution to the conception of Fig. 3. We also acknowledge Dr. Thomas Wesener, Curator, Head of Section Myriapoda at the Zoologisches Forschungsmuseum Alexander Koenig Leibniz Institute for Animal Biodiversity (Bonn, Germany) for the picture-based millipede identification, and Dr. Bobby Schopler, Supervising Veterinarian at the Duke Lemur Center (Durham, USA), and Dr. Tamara Becker, Veterinarian at the Deutsches Primatenzentrum (Göttingen, Germany), for providing information on the “sit spots”. We are also thankful to Finaritra Tolotra Randimbiarison (University of Antananarivo, Madagascar) and Dr. Matthias Markolf (Dept. Sociobiology/Anthropology, University of Göttingen, Germany) for sharing their observations. We warmly acknowledge Dr. Michael A. Huffman, Dr. Júlio César Bicca-Marques and an anonymous reviewer for their constructive comments on earlier versions of the paper. We are also thankful to Lluís Socías Martinez for his relevant comments. This study was funded by the Deutsche Forschungsgemeinschaft (DFG FI 929/21-1), (DFG FI 929/7-1), (DFG KR 3834/5-1) and the DFG research group, Sociality and health in primates (FOR2163). Field work was conducted by the German Primate Center in Kirindy with the authorization of the Commission Tripartite de la Direction des Eaux et Forêts. All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Supplementary material

Supplementary material 1 (MP4 113104 kb)

References

  1. Adamo SA, Bartlett A, Le J, Spencer N, Sullivan K (2010) Illness-induced anorexia may reduce trade-offs between digestion and immune function. Anim Behav 79:3–10CrossRefGoogle Scholar
  2. Ashwini KM, Sridhar KR (2006) Seasonal abundance and activity of pill millipedes (Arthrosphaera magna) in mixed plantation and semi-evergreen forest of southern India. Acta Oecologica 29:27–32CrossRefGoogle Scholar
  3. Bailey PT, Kovaliski J (1993) Summer quiescent behaviour of the millipede Ommatoiulus moreleti (Julida: Julidae). J Zool 231:523–532CrossRefGoogle Scholar
  4. Baker M (1996) Fur rubbing: use of medicinal plants by capuchin monkeys (Cebus capucinus). Am J Primatol 38:263–270CrossRefGoogle Scholar
  5. Barrett ADT, Higgs S (2007) Yellow fever: a disease that has yet to be conquered. Annu Rev Entomol 52:209–229CrossRefPubMedGoogle Scholar
  6. Billah MK, Kwang D, Adofo C, Adetokunbo Olu-Taiwo M, Antepim Pesewu G (2015) Antibacterial activities of millipede extracts against selected bacterial pathogens. J Microbiol Antimicrob Agents 1:30–35Google Scholar
  7. Birkinshaw CR (1999) Use of millipedes by black lemurs to anoint their bodies. Folia Primatol 70:170–171CrossRefPubMedGoogle Scholar
  8. Bowler M, Messer EJE, Claidière N, Whiten A (2015) Mutual medication in capuchin monkeys—social anointing improves coverage of topically applied anti-parasite medicines. Sci Rep 5:15030CrossRefPubMedPubMedCentralGoogle Scholar
  9. Campbell CJ (2000) Fur rubbing behavior in free-ranging black-handed spider monkeys (Ateles geoffroyi) in Panama. Am J Primatol 51:205–208CrossRefPubMedGoogle Scholar
  10. Carroll JF, Kramer M, Weldon PJ, Robbins RG (2005) Anointing chemicals and ectoparasites: effects of benzoquinones from millipedes on the lone star tick, Amblyomma americanum. J Chem Ecol 31:63–75CrossRefPubMedGoogle Scholar
  11. Clough D (2010) Gastro-intestinal parasites of red-fronted lemurs in Kirindy Forest, western Madagascar. J Parasitol 96:245–251CrossRefPubMedGoogle Scholar
  12. Costa-Neto EM (2012) Zoopharmacognosy, the self-medication behavior of animals. Interfaces Científicas Saúde e Ambiente 1:61–72CrossRefGoogle Scholar
  13. Cross JH (1996) Enteric nematodes of humans. In: Baron S (ed) Medical microbiology, 4th edn. University of Texas, Galveston. Available from: https://www.ncbi.nlm.nih.gov/books/NBK8261/. Accessed Oct 2017
  14. Dandawate PR, Vyas AC, Padhye SB, Singh MW, Baruah JB (2010) Perspectives on medicinal properties of benzoquinone compounds. Mini Rev Med Chem 10:436–454CrossRefPubMedGoogle Scholar
  15. Dangerfield JM (1998) Biology and ecology of millipedes in the Kalahari. Trans R Soc S Afr 53:183–194CrossRefGoogle Scholar
  16. David J-F, Handa IT (2010) The ecology of saprophagous macroarthropods (millipedes, woodlice) in the context of global change. Biol Rev 85:881–895PubMedGoogle Scholar
  17. Deml R, Huth A (2000) Benzoquinones and hydroquinones in defensive secretions of tropical millipedes. Naturwissenschaften 87:80–82CrossRefPubMedGoogle Scholar
  18. Doolan SP, Macdonald DW (1996) Diet and foraging behaviour of group-living meerkats, Suricata suricatta, in the southern Kalahari. J Zool 239:697–716CrossRefGoogle Scholar
  19. Enghoff H, Manno N, Tchibozo S, List M, Schwarzinger B, Schoefberger W, Schwarzinger C, Paoletti MG (2014) Millipedes as food for humans: their nutritional and possible antimalarial value—a first report. Evid Based Complement Altern Med 2014:1–9CrossRefGoogle Scholar
  20. Fichtel C, Schnoell AV, Kappeler PM (2017) Measuring social tolerance: an experimental approach in two lemurid primates. Ethology 124:65–73CrossRefGoogle Scholar
  21. Freed B (1995) A comparative ecological study of two sympatric species of primates, Lemur coronatus and Lemur fulvus sanfordi, in northern Madagascar. Doctoral dissertation. Washington University, St. LouisGoogle Scholar
  22. Gasco AD, Pérez-Acosta AM, Monticelli PF (2016) Ring-tailed coatis anointing with soap: a new variation of self-medication culture? Int J Comp Psychol 29:1–11Google Scholar
  23. Giacometti A, Cirioni O, Antonicelli L, D’Amato G, Silvestri C, Del Prete MS, Scalise G (2003) Prevalence of intestinal parasites among individuals with allergic skin diseases. J Parasitol 89:490–492CrossRefPubMedGoogle Scholar
  24. Gubler DJ (2009) Vector-borne diseases. Rev Sci Tech 28:583–588CrossRefPubMedGoogle Scholar
  25. Huffman MA (1997) Current evidence for self-medication in primates: a multidisciplinary perspective. Am J Phys Anthropol 104:171–200CrossRefGoogle Scholar
  26. Huffman MA (2007) Primate self-medication. In: Campbell C, Fuentes A, MacKinnon K, Panger M, Bearder SK (eds) Primates in perspective. Oxford University Press, Oxford, pp 677–690Google Scholar
  27. Huffman MA, Gotoh S, Turner LA, Hamai M, Yoshida K (1997) Seasonal trends in intestinal nematode infection and medicinal plant use among chimpanzees in the Mahale Mountains, Tanzania. Primates 38:111–125CrossRefGoogle Scholar
  28. Irwin MT, Raharison J-L (2009) A review of the endoparasites of the lemurs of Madagascar. Malagasy Nat 2:66–93Google Scholar
  29. Jefferson JP, Tapanes E, Evans S (2014) Owl monkeys (Aotus spp.) perform self- and social anointing in captivity. Folia Primatol 85:119–134CrossRefPubMedGoogle Scholar
  30. Jisook K (2013) Biological implications of benzoquinones. In: Price ER, Johnson SC (eds) Quinones occurrence, medicinal uses and physiological importance. Nova Science, Hauppauge, pp 57–84Google Scholar
  31. Junge RE (2006) Overview on the health and disease ecology of wild lemurs: conservation implications. In: Gould L, Sauther ML (eds) Lemurs. Springer, Boston, pp 423–440CrossRefGoogle Scholar
  32. Junge RE, Louis EE (2005) Biomedical evaluation of two sympatric lemur species (Propithecus verreauxi deckeni and Eulemur fulvus rufus) in Tsiombokibo classified forest, Madagascar. J Zoo Wildl Med 36:581–589CrossRefPubMedGoogle Scholar
  33. Junge RE, Dutton CJ, Knightly F, Williams CV, Rasambainarivo FT, Louis EE (2008) Comparison of biomedical evaluation for white-fronted brown lemurs (Eulemur fulvus albifrons) from four sites in Madagascar. J Zoo Wildl Med 39:567–575CrossRefPubMedGoogle Scholar
  34. Krief S, Hladik CM, Haxaire C (2005) Ethnomedicinal and bioactive properties of plants ingested by wild chimpanzees in Uganda. J Ethnopharmacol 101:1–15CrossRefPubMedGoogle Scholar
  35. Laska M, Bauer V, Salazar LTH (2007) Self-anointing behavior in free-ranging spider monkeys (Ateles geoffroyi) in Mexico. Primates 48:160–163CrossRefPubMedGoogle Scholar
  36. Lewis JGE (1974) The ecology of centipedes and millipedes in northern Nigeria. Symp Zool Soc Lond 32:423–431Google Scholar
  37. Lynch Alfaro JW, Matthews L, Boyette AH et al (2012) Anointing variation across wild capuchin populations: a review of material preferences, bout frequency and anointing sociality in Cebus and Sapajus: capuchin variation in anointing. Am J Primatol 74:299–314CrossRefGoogle Scholar
  38. Meredith EL (2016) Evaluating quinone based compounds for their antitrypanosomatid properties. Doctoral dissertation. Queen Mary University, LondonGoogle Scholar
  39. Morozov NS (2015) Why do birds practice anting? Biol Bull Rev 5:353–365CrossRefGoogle Scholar
  40. Morrogh-Bernard HC (2008) Fur-rubbing as a form of self-medication in Pongo pygmaeus. Int J Primatol 29:1059–1064CrossRefGoogle Scholar
  41. Overdorff DJ (1993) Similarities, differences, and seasonal patterns in the diets of Eulemur rubriventer and Eulemur fulvus rufus in the Ranomafana National Park, Madagascar. Int J Primatol 14:721–753CrossRefGoogle Scholar
  42. Parkes KC, Weldon PJ, Hoffman RL (2003) Polydesmidan millipede used in self-anointing by a strong-billed woodcreeper (Xiphocolaptes promeropirhyncus) from Belize. Ornitologia Neotropical 14:285–286Google Scholar
  43. Pereira ME, Kappeler PM (1997) Divergent systems of agonistic behaviour in lemurid primates. Behaviour 134:225–274CrossRefGoogle Scholar
  44. Poirotte C, Benhamou S, Mandjembe A, Willaume E, Kappeler PM, Charpentier M (2017) Gastrointestinal parasitism and recursive movements in free-ranging mandrills. Anim Behav 134:87–98CrossRefGoogle Scholar
  45. Roncadori RW, Duffey SS, Blum MS (1985) Antifungal activity of defensive secretions of certain millipedes. Mycologia 77:185CrossRefGoogle Scholar
  46. Santori R (1998) Discrimination of millipedes by the opossum Didelphis albiventris (Marsupialia, Didelphidae). J Adv Zool 19:118–119Google Scholar
  47. Shear WA (2015) The chemical defenses of millipedes (Diplopoda): biochemistry, physiology and ecology. Biochem Syst Ecol 61:78–117CrossRefGoogle Scholar
  48. Simmen B, Tarnaud L (2011) Utilisation des sécrétions de myriapodes chez les lémurs et les sapajous: fonction curative ou signalisation sociale? Rev Primatol 3. http://journals.openedition.org/primatologie/644. Accessed 20 Dec 2016
  49. Souza-Alves JP, Albuquerque NM, Vinhas L, Cardoso TS, Beltrão-Mendes R, Jerusalinsky L (2018) Self-anointing behaviour in captive titi monkeys (Callicebus spp.). Primate Biol 5:1–5CrossRefGoogle Scholar
  50. Springer A, Kappeler PM (2016) Intestinal parasite communities of six sympatric lemur species at Kirindy Forest, Madagascar. Primate Biol 3:51–63CrossRefGoogle Scholar
  51. Stanković S, Dimkić I, Vujisić L, Pavković-Lučić S, Jovanović Z, Stević T, Sofrenić I, Mitić B, Tomić V (2016) Chemical defence in a millipede: evaluation and characterization of antimicrobial activity of the defensive secretion from Pachyiulus hungaricus (Karsch 1881) (Diplopoda, Julida, Julidae). PLoS One 11:e0167249CrossRefPubMedPubMedCentralGoogle Scholar
  52. Telford SR, Dangerfield JM (1990) Manipulation of the sex ratio and duration of copulation in the tropical millipede Alloporus uncinatus: a test of the copulatory guarding hypothesis. Anim Behav 40:984–986CrossRefGoogle Scholar
  53. Valderrama X, Robinson JG, Attygalle AB, Eisner T (2000) Seasonal anointment with millipedes in a wild primate: a chemical defense against insects? J Chem Ecol 26:2781–2790CrossRefGoogle Scholar
  54. Varga M, Dumitraşcu D, Piloff L, Chioreanu E (2001) Skin manifestations in parasite infection. Roum Arch Microbiol Immunol 60:359–369PubMedGoogle Scholar
  55. Vasey N (2000) Niche separation in Varecia variegata rubra and Eulemur fulvus albifrons: I. Interspecific patterns. Am J Phys Anthropol 112:411–431CrossRefPubMedGoogle Scholar
  56. Vasey N (2004) Circadian rhythms in diet and habitat use in red ruffed lemurs (Varecia rubra) and white-fronted brown lemurs (Eulemur fulvus albifrons). Am J Phys Anthropol 124:353–363CrossRefPubMedGoogle Scholar
  57. Weldon PJ, Aldrich JR, Klun JA, Oliver JE, Debboun M (2003) Benzoquinones from millipedes deter mosquitoes and elicit self-anointing in capuchin monkeys (Cebus spp.). Naturwissenschaften 90:301–304CrossRefPubMedGoogle Scholar
  58. Weldon PJ, Cranmore CF, Chatfield JA (2006) Prey-rolling behavior of coatis (Nasua spp.) is elicited by benzoquinones from millipedes. Naturwissenschaften 93:14–16CrossRefPubMedGoogle Scholar
  59. Williams LAD, Singh PDA, Caleb-Williams LS (1997) Biology and biological action of the defensive secretion from a Jamaican millipede. Naturwissenschaften 84:143–144CrossRefPubMedGoogle Scholar
  60. Wu X, Buden DW, Attygalle AB (2007) Hydroquinones from defensive secretion of a giant Pacific millipede, Acladocricus setigerus (Diplopoda: Spirobolida). Chemoecology 17:131–138CrossRefGoogle Scholar
  61. Zito M, Evans S, Weldon PJ (2002) Owl monkeys (Aotus spp.) self-anoint with plants and millipedes. Folia Primatol 74:159–161CrossRefGoogle Scholar

Copyright information

© Japan Monkey Centre and Springer Japan KK, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Behavioural Ecology and Sociobiology UnitGerman Primate Center, Leibniz Institute for Primate ResearchGöttingenGermany
  2. 2.Department of Sociobiology/AnthropologyUniversity of GöttingenGöttingenGermany

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