Skip to main content Accessibility help

We use cookies to distinguish you from other users and to provide you with a better experience on our websites. Close this message to accept cookies or find out how to manage your cookie settings.

Close cookie message
×
Hostname: page-component-586b7cd67f-gb8f7 Total loading time: 0 Render date: 2024-11-22T12:37:34.602Z Has data issue: false hasContentIssue false

1 - Who are you? How lemurs recognise each other in a smell-centred world

from Part I - Communication: from sociality to society

Published online by Cambridge University Press:  05 May 2016

Ivan Norscia  and
Elisabetta Palagi
Foreword by
Alison Jolly  and
Ian Tatterall
Afterword by
Michael Huffman
Ivan Norscia
Affiliation:
Università degli Studi, Pisa
Elisabetta Palagi
Affiliation:
Università degli Studi, Pisa
Get access

Summary

He approached these faces – even of those near and dear – as if they were abstract puzzles or tests. He did not relate to them, he did not behold. No face was familiar to him, seen as a ‘thou’, being just identified as a set of features, an ‘it’. Thus, there was formal, but no trace of personal, gnosis. And with this went his indifference, or blindness, to expression. A face, to us, is a person looking out – we see, as it were, the person through his persona, his face. But for Dr P. there was no persona in this sense – no outward persona, and no person within…His absurd abstractness of attitude…which rendered him incapable of perceiving identity, or particulars, rendered him incapable of judgment.

Oliver Sacks, 1970 (p. 13)

Individual recognition: why and how

Human society is founded on individual recognition. The distinction of ‘others from others’ rules every aspect of a community, from the personal to the social level. In his ‘The Man Who Mistook His Wife for a Hat’, Oliver Sacks (1970) stresses how the ability to discern individuals is crucial to make a judgement over them and their true identity. Understanding individuals’ uniqueness is pivotal to choose partners and friends, care for family members, vote for a candidate, form political alliances, seal trade agreements, and follow rock icons or religious leaders. Individual recognition is not unique to humans. It is, instead, an ancient cognitive skill shared with other primates and rooted in humans’ mammalian history. From lemurs to apes, such ability is critical, for example, to select mates and supporters, form parent–offspring bonds, establish dominance relationships, set up coalitions, exchange or interchange commodities and follow group leaders (Thom and Hurst, 2004). Individual recognition is an excellent example of the cognitive continuity that bridges humans and other primates.

Individuals can be discriminated according to their unique features, or cues. Different from signals, specifically designed to convey information beneficial to the sender (Bradbury and Veherencamp, 1998), cues carry potential information whose relevance depends on the receiver. Paradoxically, the same cue can mean something for one animal and nothing for another which does not read the cue as a cue at all! Consequently, defining a cue is not easy.

Type
Chapter
Information
The Missing Lemur Link
An Ancestral Step in the Evolution of Human Behaviour
 , pp. 3 - 29
Publisher: Cambridge University Press
Print publication year: 2016

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abbott, D. H. (1984). Behavioral and physiological suppression of fertility in subordinate marmoset monkeys. American Journal of Primatology, 6, 169–186.Google Scholar
Adachi, I. & Fujita, K. (2007). Cross-modal representation of human caretakers in squirrel monkeys. Behavioural Processes, 74, 27–32.Google Scholar
Alvarado, J. C., Stanford, T. R., Vaughan, J. W. & Stein, B. E. (2007). Cortex mediates multisensory but not unisensory integration in superior colliculus. The Journal of Neuroscience, 27, 12775–12786.Google Scholar
Barton, R. A. (1998). Visual specialization and brain evolution in primates. Proceedings of the Royal Society B: Biological Sciences, 265, 1933–1937.Google Scholar
Bauer, H. R. & Philip, M. M. (1983). Facial and vocal individual recognition in the common chimpanzee. The Psychological Record, 33, 161–170.Google Scholar
Beacham, J. L. (2003). Models of dominance hierarchy formation: effect of prior experience and intrinsic traits. Behaviour, 140, 1275–1303.Google Scholar
Bianchet, M. A., Bains, G., Pelosi, P., et al. (1996). The three dimensional structure of bovine odorant-binding protein and its mechanism of odor recognition. Nature Structural Biology, 3, 934–939.Google Scholar
Blank, H., Anwander, A. & von Kriegstein, K. (2011). Direct structural connections between voice- and face-recognition areas. The Journal of Neuroscience, 31(36), 12906–12915.Google Scholar
Blaustein, A. R. (1981). Sexual selection and mammalian olfaction. American Naturalist, 117, 1006–1010.Google Scholar
Bradbury, J. K. & Veherencamp, S. L. (1998). Principles of Animal Communication. Sinauer Associates, Sunderland.
Bruce, V. & Young, A. (1986). Understanding face recognition. British Journal of Psychology, 77, 305–327.Google Scholar
Buck, L. & Axel, R. (1991). A novel multigene family may encode odorant receptors: a molecular basis for odor recognition. Cell, 65, 175–187.CrossRefGoogle Scholar
Campanella, S. & Belin, P. (2007). Integrating face and voice in person perception. Trends in Cognitive Sciences, 11, 535–543.CrossRefGoogle Scholar
Charpentier, M. J. E., Crawford, J. C., Boulet, M. & Drea, C. M. (2010). Message ‘scent’: lemurs detect the genetic relatedness and quality of conspecifics via olfactory cues. Animal Behaviour, 80, 101–108.Google Scholar
Clarke, P. M. R., Barrett, L. & Henzi, S. P. (2009). What role do olfactory cues play in chacma baboon mating?American Journal of Primatology, 71, 1–10.Google Scholar
Clutton-Brock, T. (2007). Sexual selection in males and females. Science, 318, 1882–1885.CrossRefGoogle Scholar
Dapporto, L. (2008). The asymmetric scent: ringtailed lemurs (Lemur catta) have distinct chemical signatures in left and right brachial glands. Naturwissenschaften, 95, 987–991.Google Scholar
Darwin, C. (1871). The Descent of Man and Selection in Relation to Sex. Murray, London.
Dawson, G. A. (1977). Composition and stability of social groups of the tamarin, Saguinus oedipus geoffroyi, in Panama: ecological and behavioral implications. In: Kleiman, D. G. (ed.), The Biology and Conservation of the Callitrichidae. Washington: Smithsonian Institution Press, pp. 23–37.
de Waal, F. B. & van Roosmalen, A. (1979). Reconciliation and consolation among chimpanzees. Behavioral Ecology and Sociobiology, 5, 55–66.Google Scholar
Delbarco-Trillo, J., Burkert, B. A., Goodwin, T. E. & Drea, C. M. (2011). Night and day: the comparative study of strepsirrhine primates reveals socioecological and phylogenetic patterns in olfactory signals. Journal of Evolutionary Biology, 24, 82–98.Google Scholar
Dugmore, S. J., Bailey, K. & Evans, C. S. (1984). Discrimination by male ring-tailed lemurs (Lemur catta) between the scent marks of male and those of female conspecifics. International Journal of Primatology, 5, 235–245.Google Scholar
Endler, J. A. (1993). Some general comments on the evolution and design of animal communication systems. Philosophical Transactions of the Royal Society of London B, 340, 215–225.CrossRefGoogle Scholar
Epple, G. (1979). Odor communication in the tamarin Saguinus fuscicollis (Callitrichidae): behavioral and chemical studies. In: Ritter, F. (ed.), Chemical Ecology: Odour Communication in Animals. Amsterdam: Elsevier/North Holland Biomedical Press, pp. 117–130.
Epple, G. (1980). Relationships between aggression, scent marking and gonadal state in a primate, the tamarin Saguinus fuscicollis. In: Müller-Schwarze, D & Silverstein, R. M. (eds), Chemical Signals – Vertebrates and Aquatic Invertebrates. New York: Plenum Press, pp. 87–105.
Epple, G., Golob, N. F., Cebul, M-S. & Smith, A. B., III (1981). Communication by scent in some Callitrichidae (Primates) – an interdisciplinary approach. Chemical Senses, 6, 377–390.Google Scholar
Epple, G., Belcher, A. M., Küderling, I, et al. (1993). Making sense out of scents: species differences in scent glands, scent-marking behaviour, and scent-mark composition in the Callitrichidae. In: Rylands, A. B. (ed.), Marmosets and Tamarins: Systematics, Behaviour, and Ecology. Oxford: Oxford University Press, pp. 123–151.
Ernst, M. O. & Bülthoff, H. H. (2004). Merging the senses into a robust percept. Trends in Cognitive Sciences, 8, 162–9.Google Scholar
Ettlinger, G. & Wilson, W. A. (1990). Cross-modal performance: Behavioural processes, phylogenetic considerations and neural mechanisms. Behavioural Brain Research, 40, 169–192.Google Scholar
Evans, T. A., Howell, S. & Westergaard, G. C. (2005). Auditory-visual cross-modal perception of communicative stimuli in tufted capuchin monkeys (Cebus apella). Journal of Experimental Psychology: Animal Behavior Processes, 31, 399–406.Google Scholar
Ferkin, M. H., Sorokin, E. S., Johnston, R. E. & Lee, C. J. (1997). Attractiveness of scents varies with protein content of the diet in meadow voles. Animal Behaviour, 53, 133–141.Google Scholar
Ferris, C. F., Snowdon, C. T., King, J. A., et al. (2001). Functional imaging of brain activity in conscious monkeys responding to sexually arousing cues. Neuroreport, 12, 2231–2236.Google Scholar
Fleagle, J. G. (2013). Primate Adaptation and Evolution, 3rd ed. San Diego: Academic Press. 596 p.
Freeman, N. J., Pasternak, G. M., Rubi, T. L., Barrett, L. & Henzi, S. P. (2012). Evidence for scent marking in vervet monkeys?Primates, 53, 311–315.Google Scholar
Geissman, T. (1987). A sternal gland in the siamang gibbon (Hylobates syndactylus). International Journal of Primatology, 8, 1–15.Google Scholar
Ghazanfar, A. A. & Logothetis, N. K. (2003). Neuroperception: facial expressions linked to monkey calls. Nature, 423, 937–938.CrossRefGoogle Scholar
Ghazanfar, A. A., Chandrasekaran, C. & Logothetis, N. K. (2008). Interactions between the superior temporal sulcus and auditory cortex mediate dynamic face/voice integration in rhesus monkeys. The Journal of Neuroscience, 28, 4457–4469.Google Scholar
Gil-da-Costa, R., Braun, A., Lopes, M., et al. (2004). Toward an evolutionary perspective on conceptual representation: Species-specific calls activate visual and affective processing systems in the macaque. PNAS, 101(50), 17516–17521.Google Scholar
Gosling, L. M. (1982). A reassessment of the function of scent marking in territories. Zeitschrift für Tierpsychologie, 60, 89–118.Google Scholar
Gosling, L. M. & Roberts, S. (2001). Testing ideas about the function of scent marks in territories from spatial patterns. Animal Behaviour, 62, F7–F10.Google Scholar
Gottfried, J. A., Smith, A. P. R., Rugg, M. D. & Dolan, R. J. (2004). Remembrance of odors past: human olfactory cortex in cross-modal recognition memory. Neuron, 42, 687–695.Google Scholar
Gould, L., Sussman, R. W. & Sauther, M. L. (2003). Demographic and life-history patterns in a population of ring-tailed lemurs (Lemur catta) at Beza Mahafaly Reserve, Madagascar: A 15-year perspective. American Journal of Physical Anthropology, 120, 182–194.Google Scholar
Green, J. A. & Gustafson, G. E. (1983). Individual recognition of human infants on the basis of cries alone. Developmental Psychobiology, 16, 485–493.CrossRefGoogle Scholar
Harrington, J. E. (1977). Discrimination between males and females by scent in Lemur fulvus. Animal Behaviour, 25, 147–151.Google Scholar
Harrington, J. E. (1979). Responses of Lemur fulvus to scents of different subspecies of L. fulvus and to scents of different species of lemuriformes. Zeitschrift für Tierpsychologie, 49, 1–9.CrossRefGoogle Scholar
Heymann, E. W. (1998). Sex differences in olfactory communication in a wild primate, Saguinus mystax (Callitrichinae). Behavioral Ecology and Sociobiology, 43, 37–45.Google Scholar
Heymann, E. W. (2000). Spatial patterns of scent marking in wild moustached tamarins, Saguinus mystax: no evidence for a territorial function. Animal Behaviour, 60, 723–730.CrossRefGoogle Scholar
Heymann, E. W. (2001). Interspecific variation of scent-marking behaviour in wild tamarins, Saguinus mystax and Saguinus fuscicollis. Folia Primatologica, 72, 253–267.Google Scholar
Heymann, E. W. (2003). Scent marking, paternal care, and sexual selection in callitrichines. In: Jones, C. B. (ed.), Sexual Selection and Reproductive Competition in Primates: New Perspectives and Directions. Norman: American Society of Primatologists, pp. 305–325.
Heymann, E. W. (2006). The neglected sense – olfaction in primate behavior, ecology, and evolution. American Journal of Primatology, 68, 519–524.Google Scholar
Heymann, E. W. (2009). Primate olfactory communication: the influence of life history and sexual selection. Folia Primatologica, 80, 370.Google Scholar
Hübener, F. & Laska, M. (1998). Assessing olfactory performance in an Old World primate, Macaca nemestrina. Physiology and Behavior, 64, 521–527.Google Scholar
Hurst, J. L. & Beynon, R. J. (2004). Scent wars: the chemobiology of competitive signaling in mice. BioEssays, 26, 1288–1298.CrossRefGoogle Scholar
Izawa, K. (1978). A field study of the ecology and behavior of the black-mantled tamarin (Saguinus nigricollis). Primates, 19, 241–274.Google Scholar
Izumi, A. & Kojima, S. (2004). Matching vocalizations to vocalizing faces in a chimpanzee (Pan troglodytes). Animal Cognition, 7(3), 179–184.Google Scholar
Jannett, F. J., Jr (1986). Morphometric patterns among microtine rodents. I. Sexual selection suggested by relative scent gland development in representative voles (Microtus). In: Duvall, D, Müller-Schwarze, D. & Silverstein, R. (eds), Chemical Signals in Vertebrates 4. New York: Plenum Press.
Joassin, F., Maurage, P. & Campanella, , , S (2011). The neural network sustaining the crossmodal processing of human gender from faces and voices: an fMRI study. Neuroimage, 54, 1654–1661.Google Scholar
Johnston, R. E. & Bullock, T. A. (2001). Individual recognition by use of odors in golden hamsters: The nature of individual representations. Animal Behaviour, 61, 545–557.Google Scholar
Johnston, R. E. & Jernigan, P. (1994). Golden hamsters recognize individuals, not just individual scents. Animal Behaviour, 48, 129–136.Google Scholar
Johnston, R. E. & Peng, A. (2008). Memory for individuals: Hamsters (Mesocricetus auratus) require contact to develop multicomponent representations (concepts) of others. Journal of Comparative Psychology, 122, 121–131.CrossRefGoogle Scholar
Jolly, A. (1966a). Lemur Behaviour: a Madagascar Field Study. Chicago: The University of Chicago Press.
Jolly, A. (1966b). Lemur social behavior and primate intelligence. Science, 153, 501–506.Google Scholar
Jolly, A. & Pride, E. (1999). Troop histories and range inertia of Lemur catta at Berenty, Madagascar: a 33-year perspective. International Journal of Primatology, 20, 359–373.Google Scholar
Kanwisher, N., McDermott, J. & Chun, M. M. (1997). The fusiform face area: a module in human extrastriate cortex specialized for face perception. The Journal of Neuroscience, 17, 4302–4311.Google Scholar
Kappeler, P. M. (1998). To whom it may concern: the transmission and function of chemical signals in Lemur catta. Behavioral Ecology and Sociobiology, 42, 411–412.Google Scholar
Kojima, S., Izumi, A. & Ceugniet, M. (2003). Identification of vocalizers by pant hoots, pant grunts and screams in a chimpanzee. Primates, 44(3), 225–230.Google Scholar
Kondo, N., Izawa, E. & Watanabe, S. (2012). Crows cross-modally recognize group members but not non-group members. Proceedings of the Royal Society B: Biological Sciences, 279, 1937–1942.Google Scholar
Krebs, J. R. & Davies, N. B. (1993). An Introduction to Behavioural Ecology, 3rd ed. Oxford: Blackwell Science.
Kulahci, I. G., Drea, C. M., Rubenstein, D. I. & Ghazanfar, A. A. (2014). Individual recognition through olfactory–auditory matching in lemurs. Proceedings of the Royal Society B: Biological Sciences, 281, 20140071.Google Scholar
Leal, W. S. (2013). Odorant reception in insects: roles of receptors, binding proteins, and degrading enzymes. Annual Review of Entomology, 58, 373–391.Google Scholar
Liebert, A. E. & Starks, P. T. (2004). The action component of recognition systems: a focus on the response. Annales Zoologici Fennici, 41, 747–764.Google Scholar
Lindsay, N. B. D. (1979). A report on the field study of Geoffroy's tamarin Saguinus oedipus geoffroyi. Dodo Journal of the Jersey Wildlife Preservation Trust, 16, 27–51.Google Scholar
Lledo Ferrer, Y., Peláez, F. & Heymann, E. W. (2011). The equivocal relationship between territoriality and scent marking in wild saddleback tamarins, Saguinus fuscicollis. International Journal of Primatology, 32, 974–991.Google Scholar
Lledo Ferrer, Y., Peláez, F. & Heymann, E. W. (2012). Territorial polemics: a response to Roberts. International Journal of Primatology, 33, 762–768.Google Scholar
Lynch Alfaro, J. W., De Sousa E Silva, J. & Rylands, A. B. (2012). How different are robust and gracile capuchin monkeys? An argument for the use of Sapajus and Cebus. American Journal of Primatology, 74, 273–286.CrossRefGoogle Scholar
Macedonia, J. M. (1986). Individuality in a contact call of the ringtailed lemur (Lemur catta). American Journal of Primatology, 11, 163–179.Google Scholar
Manai, R., Scorsone, E., Rousseau, L., et al. (2014). Grafting odorant binding proteins on diamond bio-MEMS. Biosensors and Bioelectronics, 60, 311–317.Google Scholar
Marechal, L., Genty, E. & Roeder, J. J. (2010). Recognition of faces of known individuals in two lemur species (Eulemur fulvus and E. macaco). Animal Behaviour, 79, 1157–1163.Google Scholar
Matauschek, C., Roos, C. & Heymann, E. W. (2011). Mitochondrial phylogeny of tamarins (Saguinus, Hoffmannsegg 1807) with taxonomic and biogeographic implications for the S. nigricollis species group. American Journal of Physical Anthropology, 144, 564–574.Google Scholar
Mateo, J. M. (2004). Recognition systems and biological organization: the perception component of social recognition. Annales Zoologici Fennici, 41, 729–745.Google Scholar
Matsuo, T., Sugaya, S., Yasukawa, J., Aigaki, T. & Fuyama, Y. (2007). Odorant-binding proteins OBP57d and OBP57e affect taste perception and host-plant preference in Drosophila sechellia. PLoS Biology, 5, e118.Google Scholar
Mertl, A. S. (1975). Discrimination of individuals by scent in a primate. Behavioral Biology, 14, 505–509.CrossRefGoogle Scholar
Mertl-Millhollen, A. S. (1986). Territorial scent marking by two sympatric lemur species. In: Duvall, D., Müller-Schwarze, D. and Silverstein, R. M. (eds), Chemical Signals in Vertebrates 4, New York: Plenum Press, pp. 385–395.
Neyman, P. F. (1977). Aspects of the ecology and social organization of free-ranging cotton-top tamarins (Saguinus oedipus) and the conservation status of the species. In: Kleiman, D. G. (ed.) The Biology and Conservation of the Callitrichidae. Washington: Smithsonian Institution Press, pp. 39–71.
Norscia, I. & Palagi, E. (2015). The socio-matrix reloaded: from hierarchy to dominance profile in wild lemurs. PeerJ, 3, e729. https://dx.doi.org/10.7717/peerj.729.Google Scholar
Oda, R. (1999). Scent marking and contact call production in ring-tailed lemurs (Lemur catta). Folia Primatologica, 70, 121–124.Google Scholar
Osman-Hill, W. C. (1953). Primates (Comparative Anatomy and Taxonomy). I. Strepsirhini. Edinburgh: University Press, pp. xxiv + 798.
Palagi, E. & Dapporto, L. (2006). Beyond odor discrimination: demonstrating individual recognition by scent in Lemur catta. Chemical Senses, 31(5), 437–443.Google Scholar
Palagi, E. & Dapporto, L. (2007). Females do it better. Individual recognition experiments reveal sexual dimorphism in Lemur catta (Linnaeus 1758) olfactory motivation and territorial defence. Journal of Experimental Biology, 210, 2700–2705.Google Scholar
Palagi, E. & Norscia, I. (2009). Multimodal signaling in wild Lemur catta: economic design and territorial function of urine marking. American Journal of Physical Anthropology, 139, 182–192.Google Scholar
Palagi, E. & Norscia, I. (2015). The season for peace: reconciliation in a despotic species (Lemur catta). PLoS ONE, 10, e0142150. http://dx.doi.org/10.1371/journal.pone.0142150.CrossRefGoogle Scholar
Palagi, E., Dapporto, L. & Borgognini-Tarli, , , S (2005a). The neglected scent: on the marking function of urine in Lemur catta. Behavioral Ecology and Sociobiology, 58, 437–445.Google Scholar
Palagi, E., Paoli, T. & Borgognini-Tarli, S. (2005b) Aggression and reconciliation in two captive groups of Lemur catta. International Journal of Primatology, 26, 279–294.Google Scholar
Parr, L. A. (2004). Perceptual biases for multimodal cues in chimpanzee (Pan troglodytes) affect recognition. Animal Cognition, 7, 171–178.Google Scholar
Pelosi, P. (1994). Odorant-binding proteins. Critical Reviews in Biochemistry and Molecular Biology, 29, 199–228.CrossRefGoogle Scholar
Pelosi, P. (2003). Physiological and artificial biosensors for odour recognition systems. In: Barsanti, L., Evangelista, V., Gualtieri, P., Passarelli, V. and Vestri, S. (eds), Molecular Electronics: bio-sensors and bio-computers (NATO ASI Series). Kluwer Academic Publishers.
Pelosi, P. & Maida, R. (1990). Odorant binding proteins in vertebrates and insects: similarities and possible common function. Chemical Senses, 15, 205–215.Google Scholar
Pelosi, P., Baldaccini, N. E. & Pisanelli, A. M. (1982). Identification of a specific olfactory receptor for 2-isobutyl-3-methoxypyrazine. Biochemical Journal, 201, 245–248.Google Scholar
Pelosi, P., Zhou, J.-J., Ban, L. P. & Calvello, M. (2006). Soluble proteins in insect chemical communication. Cell and Molecular Life Sciences, 63, 1658–1676.Google Scholar
Pelosi, P., Mastrogiacomo, R., Iovinella, I., Tuccori, E. & Persaud, K. C. (2013). Structure and biotechnological applications of odorant-binding proteins. Applied Microbiology and Biotechnology, 98, 61–70.Google Scholar
Pereira, M. E. & Weiss, M. L. (1991). Female mate choice, male migration, and the threat of infanticide in ringtailed lemurs. Behavioral Ecology and Sociobiology, 28, 141–152.Google Scholar
Persaud, K. C. & Pelosi, P. (1992). Sensor arrays using conducting polymers for an artificial nose. In: Gardner, J. W. & Bartlett, P. N. (eds), Sensors and Sensory Systems for an Electronic Nose, Berlin: Springer, pp. 237–256.CrossRef
Porter, R. H., Cernoch, J. M. & McLaughlin, F. J. (1983). Maternal recognition of neonates through olfactory cues. Physiology and Behavior, 30, 151–154.Google Scholar
Proops, L., McComb, K. & Reby, D. (2009). Cross-modal individual recognition in domestic horses (Equus caballus). PNAS, 106, 947–951.Google Scholar
Ramsay, N. F. & Giller, P. S. (1996). Scent-marking in ring-tailed lemurs: responses to the introduction of ‘foreign’ scent in the home range. Primates, 37, 13–23.Google Scholar
Rhodes, G., Jeffery, L., Watson, T. L., et al. (2004) Orientation-contingent face aftereffects and implications for face-coding mechanisms. Current Biology, 14, 2119–2123.Google Scholar
Roberts, S. C. (2012). On the relationship between scent-marking and territoriality in callitrichid primates. International Journal of Primatology, 33, 749–761.Google Scholar
Romanski, L. M. (2007). Representation and integration of auditory and visual stimuli in the primate ventral lateral prefrontal cortex. Cerebral Cortex, 17(Suppl 1), i61–i69.Google Scholar
Sacks, O. W. (1970). The Man Who Mistook His Wife for a Hat and Other Clinical Tales. New York:Touchstone.
Sakkalou, E. & Gattis, M. (2012). Infants infer intentions from prosody. Cognitive Development, 27, 1–16.Google Scholar
Sandler, B. H., Nikonova, L., Leal, W. S. & Clardy, J. (2000). Sexual attraction in the silkworm moth: structure of the pheromone-binding-protein-bombykol complex. Chemistry & Biology, 7, 143–151.Google Scholar
Scordato, E. S. & Drea, C. M. (2007). Scents and sensibility: information content of olfactory signals in the ringtailed lemur, Lemur catta. Animal Behaviour, 73, 301–314.Google Scholar
Sergent, J., Ohta, S. & MacDonald, B. (1992). Functional neuroanatomy of face and object processing: a positron emission tomography study. Brain, 115, 15–36.Google Scholar
Setchell, J. M., Vaglio, S., Moggi-Cecchi, J., et al. (2010a) Chemical composition of scent-gland secretions in an Old World monkey (Mandrillus sphinx): influence of sex, male status and individual identity. Chemical Senses, 35, 205–220.Google Scholar
Setchell, J. M., Charpentier, M. J. E., Abbott, K. M., Wickings, E. J. & Knapp, L. A. (2010b) Opposites attract: MHC-associated mate choice in a polygynous primate. Journal of Evolutionary Biology, 23, 136–148.Google Scholar
Setchell, J. M., Vaglio, S., Abbott, K. M., et al. (2011). Odour signals major histocompatibility complex genotype in an Old World monkey. Proceedings of the Royal Society B: Biological Sciences, 278, 274–280.Google Scholar
Seyfarth, R. M. & Cheney, D. L. (2009). Seeing who we hear and hearing who we see. PNAS, 106, 669–670.Google Scholar
Sliwa, J., Duhamel, J. R., Pascalis, O. & Wirth, S. (2011). Spontaneous voice-face identity matching by rhesus monkeys for familiar conspecifics and humans. PNAS, 108, 1735–1740.Google Scholar
Smith, T. E., Tomlinson, A. J., Mlotkiewicz, J. A. & Abbott, D. H. (2001). Female marmoset monkeys (Callithrix jacchus) can be identified from the chemical composition of their scent marks. Chemical Senses, 26, 449–458.Google Scholar
Sprankel, H. (1961). Histologie und biologische Bedeutung eines jugulo-sternalen Duftdrüsenfeldes bei Tupaia glis Diard 1820. Verhandlungen der Deutschen Zoologischen Gesellschaft, 25, 198–206.Google Scholar
Sprankel, H. (1971). Zur vergleichenden Histologie von Hautdrüsenorganen im Lippenbereich bei Tarsius bancanus borneanus Horsfield 1821 und Tarsius syrichta carbonarius Linnaeus 1758. In: Kummer, H (ed.), Proceedings of the 3rd International Congress of Primatology, Zurich (1970), vol 1. S. Karger, Basel, pp. 189–197.
Stitzel, S. E., Aernecke, M. J. & Walt, D. R. (2011). Artificial noses. Annual Review of Biomedical Engineering, 13, 1–25.Google Scholar
Sun, Y. F., De Biasio, F., Qiao, H. L., et al. (2012) Two odorant-binding proteins mediate the behavioural response of aphids to the alarm pheromone (E)-ß-farnesene and structural analogues. PLoS ONE, 7, e32759http://dx.doi.org/10.1371/journal.pone.0032759.Google Scholar
Swarup, S., Williams, T. I. & Anholt, R. R. (2011). Functional dissection of Odorant binding protein genes in Drosophila melanogaster. Genes, Brain and Behavior, 10, 648–657.Google Scholar
Tattersall, I. (1982). The Primates of Madagascar. New York: Columbia University Press.
Tegoni, M., Ramoni, R., Bignetti, E., Spinelli, S. & Cambillau, C. (1996). Domain swapping creates a third putative combining site in bovine odorant binding protein dimer. Nature Structual Biology, 3, 863–867.CrossRefGoogle Scholar
Tegoni, M., Campanacci, V. & Cambillau, C. (2004). Structural aspects of sexual attraction and chemical communication in insects. Trends in Biochemical Sciences, 29, 257–264.Google Scholar
Terborgh, J. (1983). Five New World Primates: A Study in Comparative Ecology. Princeton: Princeton University Press,
Terborgh, J. & Goldizen, A. W. (1985). On the mating system of the cooperatively breeding saddle-back tamarin (Saguinus fuscicollis). Behavioral Ecology and Sociobiology, 16, 293–299.Google Scholar
Thom, M. D. & Hurst, J. L. (2004). Individual recognition by scent. Annales Zoologici Fennici, 41, 765–787.Google Scholar
Trivers, R. L. (1971). Parental investment and sexual selection. In: Campbell, B. (ed.), Sexual Selection and the Descent of Man. Chicago: Aldine, pp. 139–179.
Tsutsui, N. E. (2004). Scent of self: the expression component of self/non-self recognition systems. Annales Zoologici Fennici, 41, 713–727.Google Scholar
Turner, A. P. & Magan, N. (2004). Electronic noses and disease diagnostics. Nature Reviews Microbiology, 2, 161–166.Google Scholar
Vick, L. G. & Pereira, M. E. (1989). Episodic targeting aggression and the histories of Lemur social groups. Behavioral Ecology and Sociobiology, 25, 3–12.CrossRefGoogle Scholar
Vieira, F. G. & Rozas, J. (2011). Comparative genomics of the odorant-binding and chemosensory protein gene families across the Arthropoda: Origin and evolutionary history of the chemosensory system. Genome Biology and Evolution, 3, 476–490.Google Scholar
Vogt, R. G. & Riddiford, L. M. (1981). Pheromone binding and inactivation by moth antennae. Nature, 293, 161–163.Google Scholar
Wyatt, T. D. (2014). Pheromones and Animal Behavior, 2nd Edition. Cambridge University Press, 424 pages.
Xu, P., Atkinson, R., Jones, D. N. & Smith, D. P. (2005). Drosophila OBP LUSH is required for activity of pheromone-sensitive neurons. Neuron, 45, 193–200.Google Scholar
Zala, S. M., Potts, W. K. & Penn, D. J. (2004). Scent-marking displays provide honest signals of health and infection. Behavioral Ecology, 15, 338–344.CrossRefGoogle Scholar

Save book to Kindle

To save this book to your Kindle, first ensure [email protected] is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about saving to your Kindle.

Note you can select to save to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be saved to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Available formats
×

Save book to Dropbox

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Dropbox.

Available formats
×

Save book to Google Drive

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Google Drive.

Available formats
×