Skip to main content
Log in

The neglected scent: on the marking function of urine in Lemur catta

  • Original Article
  • Published:
Behavioral Ecology and Sociobiology Aims and scope Submit manuscript

Abstract

In ring-tailed lemurs (Lemur catta) urine deposition can be combined with two different tail configurations: (i) tail held up in an evident display (urinate tail-up, UT-up); (ii) tail slightly raised to avoid its impregnation with urine (urinate tail-down, UT-down). We used both signaller- and receiver-based approaches to search for functional differences between these two kinds of urine deposition. We predicted that UT-up might be a complex signal combining olfactory and visual cues. We carried out observations and scent tests on four captive groups of ring-tailed lemurs. Group members sniffed/licked UT-up scents more frequently than UT-down ones. Moreover, UT-up showed peak levels during the mating season whereas UT-down did not. These findings suggest that urine can play a role in intra-group reproductive communication. Lemurs more frequently performed UT-up in a few drops and UT-down in streams. Recognition experiments clearly showed that individuals can discriminate between urine of their own group and urine from a foreign group (a necessary prerequisite for the use of urine in inter-group communication). The possible function of UT-up in inter-troop communication was supported by the higher frequency of this pattern along a fence separating two of the study groups. Moreover, in the presence of a dummy, the frequency of UT-up increased significantly. In conclusion, UT-up is a complex signal with multiple characteristics. By using different sensory channels, UT-up provides different types of information (location and signaller quality) and contains multiple messages directed both at group-members and neighbouring groups.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Albone ES (1984) Mammalian semiochemistry: the investigation of chemical signals between mammals. Wiley, New York

    Google Scholar 

  • Altman J (1974) Observational study of behaviour: sampling methods. Behaviour 49:227–267

    CAS  PubMed  Google Scholar 

  • Begg CM, Begg KS, Du Toit JT, Mills MGL (2003) Scent-marking behaviour of the honey badger, Mellivora capensis (Mustelidae), in the southern Kalahari. Anim Behav 66:917–929

    Article  Google Scholar 

  • Biggins JG (1984) Communication in possums: A review. In: Smith AP, Hume ID (eds) Possums and gliders. Australian Mammal Society, Sydney, pp 35–57

    Google Scholar 

  • Box HO (1977) Quantitative data on the carrying of young captive monkey (Callithrix jacchus) by other members of their family groups. Primates 18:475–484

    Google Scholar 

  • Bradbury JK, Vehrencamp SL (1998) Principles of animal communication. Sinauer Associates, Sunderland

    Google Scholar 

  • Brockman DK, Whitten PL (1996) Reproduction in free-ranging Propithecus verrauxi: Estrus and the relationship between multiple partner matings and fertilization. Am J Phys Anthropol 100:57–69

    Article  CAS  PubMed  Google Scholar 

  • Brown RE, MacDonald DW (1985) Social odours in mammals, vol. 2. Clarendon, Oxford

    Google Scholar 

  • Buesching CD, Macdonald DW (2001) Scent-marking behaviour of the European badger (Meles meles): Resource defence or individual advertisement? In: Marchlewska-Koj J, Lepri J, Müller-Schwarze D (eds) Chemical signals in vertebrates. Plenum Press, Oxford

    Google Scholar 

  • Buesching CD, Newman C, Macdonald DW (2002a) Variations in colour and volume of the subcaudal gland secretion of badgers (Meles meles) in relation to sex, season and individual-specific parameters. Mammal Biol 67:147–156

    Google Scholar 

  • Buesching CD, Waterhouse JS, Macdonald DW (2002b) Gas-chromatographic analysis of the subcaudal gland secretion of the European badger (Meles meles) part II: Time-related variation in the individual-specific composition. J Chem Ecol 28:57–69

    Article  CAS  PubMed  Google Scholar 

  • Burt WH (1943) Territoriality and home range concepts applied to mammals. J Mammal 24:346–352

    Google Scholar 

  • Chandler CF (1975) Development and function of marking and sexual behaviour in the Malagasy prosimian primate, Lemur fulvus. Primates 16:35–47

    Google Scholar 

  • Curtis DJ, Zaramody A, Green DI, Pickard AR (2000) Non-invasive monitoring of reproductive status in wild mongoose lemurs (Eulemur mongoz). Repr Fert Dev 12:21–29

    Article  CAS  Google Scholar 

  • Dawkins MS, Guilford T (1994) Design of an intention signal in the bluehead wrasse (Thalassoma bifasciatum). Proc R Soc Lond B 257:123–128

    Google Scholar 

  • Desjardins C, Maruniak JA, Bronson FH (1973) Social rank in house mice: differentiation revealed by ultraviolet visualization of urinary marking patterns. Science 182:939–941

    CAS  PubMed  Google Scholar 

  • Devenport L, Devenport J, Kokesh C (1999) The role of urine marking in the foraging behaviour of least chipmunks. Anim Behav 57:557–563

    Article  PubMed  Google Scholar 

  • Dugmore SJ, Bailey K, Evans C (1984) Discrimination by male ring-tailed lemurs (Lemur catta) between the scent marks of male and female conspecifics. Int J Primatol 5:235–245

    Google Scholar 

  • Epple G (1970) Quantitative studies on scent marking in the marmoset (Callithrix jacchus jacchus). Folia Primatol 13:48–62

    CAS  PubMed  Google Scholar 

  • Epple G (1986) Communication by chemical signals. In: Mitchell G, Erwin J (eds) Comparative primate biology 2A. Liss, New York, pp 531–580

    Google Scholar 

  • Estes RD (1969) Territorial behavior of the wildebeest (Connochaetes taurinus Burchell 1832). Z Tierpsychol 26:284–370

    Google Scholar 

  • Evans CS, Goy RW (1968) Social behaviour and reproductive cycles in captive ring-tailed lemurs (Lemur catta). J Zool 156:181–197

    Google Scholar 

  • Fisher HS, Swaisgood RR, Fitch-Snyder H (2003) Countermarking by male pygmy lorises (Nycticebus pygmaeus): do females use odour cues to select mates with high competitive ability? Behav Ecol Sociobiol 53:123–130

    Google Scholar 

  • Fornasieri I, Roeder JJ (1992) Marking behaviour in two lemur species (L. fulvus and L. macaco): relation to social status, reproduction, aggression and environmental change. Folia Primatol 59:137–148

    CAS  PubMed  Google Scholar 

  • French JA, Cleveland J (1984). Scent-marking in the tamarin, Saguinus oedipus: Sex differences and ontogeny. Anim Behav 32:615–623

    Google Scholar 

  • Gosling LM, (1986) Economic consequences of scent marking in mammalian territoriality. In: Duvall D, Müller-Schwarze D, Silverstein RM (eds) Chemical signals in vertebrates 4. Plenum Press, New York, pp 385–395

    Google Scholar 

  • Gosling LM, (1990) Scent-marking by resource holders: alternative mechanisms for advertising the costs of competition. In: MacDonald DW, Muller- Schwarze D, Natynczuk E (eds) Chemical signals in vertebrates 5. Oxford University Press, Oxford, pp 315–328

    Google Scholar 

  • Gosling LM, Roberts SC (2001). Scent-marking by male mammals: cheat-proof signals to competitors and mates. Adv Stud Behav 30:169–217

    Article  Google Scholar 

  • Gosling LM, Wright KHM (1994) Scent marking and resource defence by male coypus (Myocastor coypus). J Zool 234:423–436

    Google Scholar 

  • Guilford T, Dawkins MS (1991) Receiver psychology and the evolution of animal signals. Anim Behav 42:1–14

    Google Scholar 

  • Harrington JE (1976) Discrimination between individuals by scent in Lemur fulvus. Anim Behav 24:207–212

    CAS  PubMed  Google Scholar 

  • Harrington JE (1979) Responses of Lemur fulvus to scents of different subspecies of L. fulvus and to scents of different species of lemuriformes. Z Tierpsychol 49:1–9

    Google Scholar 

  • Hebets A, Papaj DR (2005) Complex signal function: developing a framework of testable hypotheses. Behav Ecol Sociobiol 57:197–214

    Article  Google Scholar 

  • Henry JD (1977) The use of urine marking in the scavenging behaviour of the red fox (Vulpes vulpes). Behaviour 62:82–105

    Google Scholar 

  • Hurst JL (1989) The complex network of olfactory communication in populations of wild house mice Mus musculus Rutty: urine marking and investigation within family groups. Anim Behav 37:705–725

    Article  Google Scholar 

  • Hurst JL (1990) Urine marking in populations of wild house mice Mus musculus Rutty. I. Communication between males. Anim Behav 40:209–222

    Google Scholar 

  • Irwin MT, Samonds KE, Raharison J, Write PC (2004) Lemur latrines: observations of latrine behaviour in wild primates and possible ecological significance. J Mammal 85:420–427

    Article  Google Scholar 

  • Johnson RP (1973) Scent marking in mammals. Anim Behav 21:521–535

    Google Scholar 

  • Johnstone RA (1996) Multiple displays in animal communication: “backup signals” and “multiple messages”. Philos T Roy Soc B 351:329–338

    Google Scholar 

  • Jolly A (1966) Lemur behaviour: a madagascar field study. The University of Chicago Press, Chicago

    Google Scholar 

  • Jolly A. (1967) Breeding synchrony in wild Lemur catta. In: Altmann SA (eds) Social communication among primates. The University of Chicago Press, Chicago, pp 3–13

    Google Scholar 

  • Jolly A, Oliver WLR, O’Connor SM (1982) Population and troop ranges of Lemur catta and Lemur fulvus at Berenty, Madagascar: 1980 census. Folia Primatol 39:115–123

    CAS  PubMed  Google Scholar 

  • Jolly A, Rasamimanana HR, Kinnarid MF, O’Brien TG, Crowley HM, Harcourt CS, Gardner S, Davidson JM (1993) Territoriality in Lemur catta groups during the birth season at Berenty, Madagascar. In: Kappeler PM, Ganzhorn J (eds) Lemur social systems and their ecological basis. Plenum Press, New York, London, pp 85–109

    Google Scholar 

  • Kappeler PM (1998) To whom it may concern: the transmission and function of chemical signals in Lemur catta. Behav Ecol Sociobiol 42:411–421

    Article  Google Scholar 

  • Kruuk H (1978) Social organization and social behaviour of the European badger Meles meles. J Zool 185:205–212

    Google Scholar 

  • Kruuk H, Gorman M, Leitch A (1984) Scent-marking with the subcaudal gland by the European badger, Meles meles. Anim Behav 32:899–907

    Google Scholar 

  • MacDonald DW (1985) The carnivores: Order Carnivora. In: Brown RE, MacDonald DW (eds) Social odours in mammals. Clarendon Press, Oxford, pp 619–722

    Google Scholar 

  • Markl H (1983) Vibrational communication. In: Huber R, Markl H (eds) Neuroethology and behavioral physiology. Springer, Berlin Heidelberg New York, pp 332–353

    Google Scholar 

  • Martin P, Bateson P (1993) Measuring behaviour: an introductory guide, 2nd edn. Cambridge University Press, Cambridge

    Google Scholar 

  • Mertl AS (1975) Discrimination of individuals by scent in a primate. Behav Ecol 14:505–509

    CAS  Google Scholar 

  • Mertl AS (1976) Olfactory and visul cues in social interactions of Lemur catta. Folia Primatol 26:151–161

    PubMed  Google Scholar 

  • Mertl-Millhollen AS (1986) Territorial scent marking by two sympatric lemur species. In: Duvall D, Müller-Schwarze D, Silverstein RM (eds) Chemical signals in vertebrates 4. Plenum Press, New York, pp 385–395

    Google Scholar 

  • Mertl-Millhollen AS (1988) Olfactory demarcation of territorial but not home range boundaries by Lemur catta. Folia Primatol 50:175–187

    CAS  PubMed  Google Scholar 

  • Mert-Millhollen AS, Gustafson HL, Budnitz N, Dainis K, Jolly A (1979) Population and territory stability of the Lemur catta at Berenty, Madagascar. Folia Primatol 31:106–122

    PubMed  Google Scholar 

  • Mugford RA, Nowell NW (1971) The preputial gland as a source of aggression promoting odour in mice. Physiol Behav 6:247–249

    Article  CAS  PubMed  Google Scholar 

  • Mundry R, Fischer J (1998) Use of statistical programs for nonparametric tests of small samples often lead to incorrect P values: examples from Animal Behaviour. Anim Behav 56:256–259

    Article  PubMed  Google Scholar 

  • Nievergelt CM, Mutschler T, Feistner ATC (1998) Group encounters and territoriality in wild Alaotran gentle lemurs (Hapalemur griseus alaotrensis). Am J Primatol 46:251–258

    Article  CAS  PubMed  Google Scholar 

  • Palagi E, Telara S, Borgognini Tarli SM (2003) Sniffing behaviour in Lemur catta: seasonality, sex, and rank. Int J Primatol 24:335–350

    Article  Google Scholar 

  • Palagi E, Telara S, Borgognini Tarli SM (2004) Reproductive strategies in Lemur catta: the balance among sending, receiving, and counter-marking scent signals. Int J Primatol 25:1019–1031

    Article  Google Scholar 

  • Pereira ME, Kappeler PM (1997) Divergent systems of agonistic behaviour in lemurid primates. Behaviour 134:225–274

    Google Scholar 

  • Ramsay NF, Giller PS (1996) Scent-marking in ring-tailed lemurs: responses to the introduction of “foreign” scent in the home range. Primates 37:13–23

    Google Scholar 

  • Raymer JD, Weisler D, Novotny M, Asa C, Seal US, Mech LD (1983) Volatile constituents of wolf (Canis lupus) urine as related to gender and season. Experientia 40:707–709

    Google Scholar 

  • Rosell F, Bergan F, Parker H (1998) Scent-marking in the Eurasian beaver (Castor fiber) as a means of territory defence. J Chem Ecol 24:207–219

    Article  CAS  Google Scholar 

  • Rowe C (1999) Receiver psychology and the evolution of multicomponent signals. Anim Behav 58:921–931

    PubMed  Google Scholar 

  • Rowe C, Guilford T (1999) Novelty in a multimodal warning signal. Anim Behav 57:341–346

    Article  PubMed  Google Scholar 

  • Sauther ML (1991) Reproductive behaviour of free-ranging Lemur catta at Beza Mahafaly special reserve, Madagascar. Am J Phys Anthropol 84:463–477

    Google Scholar 

  • Sauther ML, Sussman RW, Gould L (1999) The socioecology of the ring-tailed lemur: Thirty-five years of research. Evol Anthropol 8:120–132

    Article  Google Scholar 

  • Schilling A (1979) Olfactory communication in prosimians. In: Doyle GA, Martin RD (eds) The study of prosimian behaviour. Academic press, New York, pp 461–542

    Google Scholar 

  • Siegel S, Castellan NJ Jr (1988) Nonparametric statistics for the behavioural sciences. McGraw-Hill, New York

    Google Scholar 

  • Sussman RW (1974) Ecological distinctions in sympatric species of Lemur. In: Martin RD, Doyle GA, Walker AC (eds) Prosimians biology. Gerald Duckworth, London, pp 75–108

    Google Scholar 

  • Van Horn RN (1975) Primate breeding season: photoperiodic regulation in Lemur catta. Folia Primatol 24:203–220

    PubMed  Google Scholar 

  • Van Horn RN (1980) Seasonal reproductive patterns in primates. Prog Reprod Biol 5:181–221

    Google Scholar 

  • Wilson EO (1975) Sociobiology: the new synthesis. Belknap University Press, Cambridge

    Google Scholar 

  • Zub K, Theuerkauf J, Jedrzejewski W, Jedrzejewska B, Schmidt K, Kowalczyk R (2003) Wolf pack territory marking in the Bialowieza primeval forest (Poland). Behaviour 140:635–648

    Article  Google Scholar 

Download references

Acknowledgments

Thanks are due to Paolo Cavicchio (Giardino Zoologico Città di Pistoia, Pistoia, Italy), Iole Palanca, Renato Piccinini (Parco Zoo di Falconara, Falconara Marittima, AN, Italy), Maria Rodeano (Parco Zoo Punta Verde, Lignano Sabbiadoro, UD, Italy) for allowing and facilitating this work, Ruth Curreli, Sabrina Telara and Alessandro Pardini for helping with data collection, Eckhard Heymann and Anne Mertl for their critical revision, Peter Kappeler and two anonymous referees for improving the manuscript, Tommaso Paoli and Ivan Norscia for useful suggestions, and to Isabel Behncke for language revision. This research was funded by Giardino Zoologico Città di Pistoia, Parco Zoo di Falconara, Parco Zoo Punta Verde, and the University of Pisa. All the experimental procedures conformed to Italian law

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to E. Palagi.

Additional information

Communicated by P. Kappeler

“...to conceal this letter, the Minister had resorted to the comprehensive and sagacious expedient of not attempting to conceal it at all” (from the Purloined letter E. A. Poe, 1845)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Palagi, E., Dapporto, L. & Borgognini Tarli, S. The neglected scent: on the marking function of urine in Lemur catta. Behav Ecol Sociobiol 58, 437–445 (2005). https://doi.org/10.1007/s00265-005-0963-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00265-005-0963-1

Keywords

Navigation