Skip to main content
SpringerLink
Log in

Sensory information and associative cues used in food detection by wild vervet monkeys

  • Original Paper
  • Published:
Animal Cognition Aims and scope Submit manuscript

Abstract

Understanding animals’ spatial perception is a critical step toward discerning their cognitive processes. The spatial sense is multimodal and based on both the external world and mental representations of that world. Navigation in each species depends upon its evolutionary history, physiology, and ecological niche. We carried out foraging experiments on wild vervet monkeys (Chlorocebus pygerythrus) at Lake Nabugabo, Uganda, to determine the types of cues used to detect food and whether associative cues could be used to find hidden food. Our first and second set of experiments differentiated between vervets’ use of global spatial cues (including the arrangement of feeding platforms within the surrounding vegetation) and/or local layout cues (the position of platforms relative to one another), relative to the use of goal-object cues on each platform. Our third experiment provided an associative cue to the presence of food with global spatial, local layout, and goal-object cues disguised. Vervets located food above chance levels when goal-object cues and associative cues were present, and visual signals were the predominant goal-object cues that they attended to. With similar sample sizes and methods as previous studies on New World monkeys, vervets were not able to locate food using only global spatial cues and local layout cues, unlike all five species of platyrrhines thus far tested. Relative to these platyrrhines, the spatial location of food may need to stay the same for a longer time period before vervets encode this information, and goal-object cues may be more salient for them in small-scale space.

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

Access this article

Log in via an institution

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

Similar content being viewed by others

References

  • Andrews MW (1988) Selection of food sites by Callicebus moloch and Saimiri sciureus under spatially and temporally varying food distribution. Learn Motiv 19:254–268

    Article  Google Scholar 

  • Asensio N, Brockelman WY, Malaivijitnond S, Reichard UH (2011) Gibbon travel paths are goal oriented. Anim Cogn 14:395–405

    Article  PubMed  Google Scholar 

  • Balda RP, Turek RJ (1984) The cache-recovery system as an example of memory capabilities in Clark’s nutcrackers. In: Roiblat HL, Bever TG, Terrace HS (eds) Animal cognition. Erlbaum, Hillsdale, pp 513–532

    Google Scholar 

  • Barton RA (2006) Olfactory evolution and behavioral ecology in primates. Am J Primatol 68:545–558

    Article  PubMed  Google Scholar 

  • Bicca-Marques JC (2005) The win-stay rule in within-patch foraging decisions in free-ranging titi monkeys (Callicebus cupreus cupreus) and tamarins (Saguinus imperator imperator and S. fuscicollis weddelli). J Comp Psychol 119:343–351

    Article  PubMed  Google Scholar 

  • Bicca-Marques JC, Garber PA (2004) Use of spatial, visual, and olfactory information during foraging in wild nocturnal and diurnal anthropoids: a field experiment comparing Aotus, Callicebus, and Saguinus. Am J Primatol 62:171–187

    Article  PubMed  Google Scholar 

  • Brodbeck DR (1994) Memory for spatial and local cues: a comparison of a storing and nonstoring species. Anim Learn Behav 22:119–133

    Article  Google Scholar 

  • Burgess N (2006) Spatial memory: how egocentric and allocentric combine. Trends Cogn Sci 10:551–557

    Article  PubMed  Google Scholar 

  • Byrne RW (2000) How monkeys find their way: leaderships, coordination, and cognitive maps of African baboons. In: Boinski Sue, Garber Paul A (eds) On the move: how and why animals travel in groups. Academic Press, London, pp 239–264

    Google Scholar 

  • Byrne RW, Noser R, Bates LA, Jupp PE (2009) How did they get here from there? Detecting changes of direction in terrestrial ranging. Anim Behav 77:619–631

    Article  Google Scholar 

  • Cain P, Malwal S (2002) Landmark use and development of navigational behaviour in the weakly electric fish Gnathoneus petersii (Mormyridae; Teleostei). J Exper Biol 205:3915–3923

    Google Scholar 

  • Caine NG, Mundy NI (2000) Demonstration of a foraging advantage for trichromatic marmosets (Callithrix geoffroyi) dependent on food colour. Proc R Soc Lond B Biol Sci 267:439–444

    Article  CAS  Google Scholar 

  • Cartwright BA, Collett TS (1983) Landmark learning in bees: experiments and models. J Comp Physiol A 151:521–543

    Article  Google Scholar 

  • Charles-Dominique P (1977) Ecology and behaviour of nocturnal primates. Columbia University Press, New York

    Google Scholar 

  • Cheney DL, Seyfarth RM (1992) How monkeys see the world. University of Chicago Press, Chicago

    Google Scholar 

  • Cheng K (1986) A purely geometric module in the rat’s spatial representation. Cognition 23:149–178

    Article  PubMed  CAS  Google Scholar 

  • Cheng K (1989) The vector sum model of pigeon landmark use. J Exp Psychol 15:366–375

    Google Scholar 

  • Cheng K, Sherry DF (1992) Landmark-based spatial memory in birds (Parus atricapillus and Columba livia): the use of edges and distances to represent spatial positions. J Comp Psychol 106:331–341

    Article  Google Scholar 

  • Collett TS, Cartwright BA, Smith BA (1986) Landmark learning and visuo-spatial memories in gerbils. J Comp Physiol A 158:835–851

    Article  PubMed  CAS  Google Scholar 

  • Colquhoun IC (2011) A review and interspecific comparison of nocturnal and cathemeral strepsirhine primate olfactory behavioural ecology. Int J Zool 2011:1–11

    Article  Google Scholar 

  • Cramer AE, Gallistel CR (1997) Vervet monkeys as travelling salesmen. Nature 387:464

    Article  PubMed  CAS  Google Scholar 

  • Cunningham EP, Janson CH (2007) Integrating information about location and value of resources by white-faced saki monkeys (Pithecia pithecia). Anim Cogn 10:293–304

    Article  PubMed  Google Scholar 

  • Dolins FL (2009) Captive cotton-top tamarins’ (Saguinus oedipus oedipus) use of landmarks to localize hidden food items. Am J Primatol 71:316–323

    Article  PubMed  Google Scholar 

  • Dolins FL, Mitchell RW (2010) Linking spatial cognition and spatial perception. In: Dolins FL, Mitchell RW (eds) Spatial cognition, spatial perception: mapping the self and space. Cambridge University Press, UK, pp 1–31

    Google Scholar 

  • Døving KB, Trotier D (1998) Structure and function of the vomeronasal organ. J Exp Biol 201:2913–2925

    PubMed  Google Scholar 

  • Enstam Jaffe K, Isbell LA (2009) After the fire: benefits of reduced ground cover for vervet monkeys (Cercopithecus aethiops). Am J Primatol 71:252–260

    Article  Google Scholar 

  • Erhart EM, Overdorff DJ (2008) Spatial memory during foraging in Prosimian primates: Propithecus edwardsi and Eulemur fulvus rufus. Folia Primatol 79:185–196

    Article  PubMed  Google Scholar 

  • Estes RD (1992) Behaviour guide to African mammals. University of California Press, Los Angeles

    Google Scholar 

  • Etienne AS (1987) The control of short-distance homing in the golden hamster. In: Ellen P, Thinus-Blanc C (eds) Cognitive processes and spatial orientation in animal and man, vol 1., Experimental animal psychology and ethologyMartinus Nijohoff, Dordrectht, pp 233–251

    Chapter  Google Scholar 

  • Etienne AS, Maurer R, Saucy F (1988) Limitations in the assessment of path dependent information. Behaviour 106:81–111

    Article  Google Scholar 

  • Etienne AS, Berlie J, Georgakopoulos J, Maurer R (1998) Role of dead reckoning in navigation. In: Healy S (ed) Spatial representations in animals. Oxford University Press, Oxford, pp 54–68

    Google Scholar 

  • Foo P, Warren WH, Duchon A, Tarr MJ (2005) Do humans integrate routes into a cognitive map? Map- versus landmark-based navigation of novel shortcuts. J Exp Psychol 31:195–215

    Google Scholar 

  • Gallistel CR (1990) The organization of learning. MIT Press, Cambridge

    Google Scholar 

  • Gallistel CR (2009) The importance of proving the null. Psychol Rev 116:439–453

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Garber P (1989) Role of spatial memory in primate foraging patterns: Saguinus mystax and Sagunius fuscicollis. Am J Primatol 19:203–216

    Article  Google Scholar 

  • Garber PA (2000) The ecology of group movement: evidence for the use of spatial, temporal, and social information by some primate foragers. In: Boinski S, Garber PA (eds) On the move: how and why animals travel in groups. Chicago University Press, Chicago, pp 261–298

    Google Scholar 

  • Garber PA, Brown E (2006) Use of landmark cues to locate feeding sites in wild capuchin monkeys (Cebus capucinus): an experimental field study. In: Estrada A, Garber PA, Pavelka MSM, Luecke L (eds) New perspectives in the study of Mesoamerican primates. Springer, New York, pp 311–332

    Chapter  Google Scholar 

  • Garber PA, Dolins FL (1996) Testing learning paradigms in the field: evidence for use of spatial and perceptual information and rule-based foraging in wild moustached tamarins. In: Norconk MA, Rosenberger AL, Garber PA (eds) Adaptive radiation of neotropical primates. Plenum Press, New York, pp 201–216

    Chapter  Google Scholar 

  • Garber PA, Lavallee A (1999) Experimental approaches to the study of primate cognition in natural and near-to-wild field settings. In: Garber PA, Leigh S (eds) Readings in the biological bases of human behavior. Pearson Custom Publishers, Massachusetts, pp 71–98

    Google Scholar 

  • Garber PA, Paciulli LM (1997) Experimental field study of spatial memory and learning in wild capuchin monkeys (Cebus capucinus). Folia Primatol 68:236–253

    Article  PubMed  CAS  Google Scholar 

  • Groves C (2001) Primate taxonomy. Smithsonian, Washington

    Google Scholar 

  • Hermer L, Spelke ES (1994) A geometric process for spatial reorientation in young children. Nature 370:57–59

    Article  PubMed  CAS  Google Scholar 

  • Hribar A, Call J (2011) Great apes use landmark cues over spatial relations to find hidden food. Anim Cogn 14:623–635

    Article  PubMed  Google Scholar 

  • Isbell LA (2009) The fruit, the tree, and the serpent: why we see so well. Harvard University Press, Cambridge

    Google Scholar 

  • Isbell LA, Pruetz JD, Young TP (1998) Movements of vervets (Cercopithecus aethiops) and patas monkeys (Erythrocebus patas) as estimators of food resource size, density, and distribution. Behav Ecol Sociobiol 42:123–133

    Article  Google Scholar 

  • Jacobs GH (2009) Evolution of colour vision in mammals. Phil Trans R Soc Lond B 364:2957–2967

    Article  CAS  Google Scholar 

  • Jacobs GH, Neitz M, Neitz J (1996) Mutations in S-cone pigment genes and the absence of colour vision in two species of nocturnal primate. Proc R Soc Lond B Biol Sci 263:705–710

    Article  CAS  Google Scholar 

  • Janmaat KRL, Byrne RW, Zuberbühler K (2006a) Evidence for a spatial memory of fruiting states of rainforest trees in wild mangabeys. Anim Behav 72:797–807

    Article  Google Scholar 

  • Janmaat KRL, Byrne RW, Zuberbühler K (2006b) Primates take weather into account when searching for fruits. Curr Biol 16:1232–1237

    Article  PubMed  CAS  Google Scholar 

  • Janson CH (1996) Towards an experimental socioecology of primates: examples for Argentine brown capuchin monkeys (Cebus apella nigritus). In: Norconk MA, Rosenberger AL, Garber PA (eds) Adaptive radiation of neotropical primates. Plenum Press, New York, pp 309–325

    Chapter  Google Scholar 

  • Janson CH (2007) Experimental evidence for route integration and strategic planning in wild capuchin monkeys. Anim Cogn 10:341–356

    Article  PubMed  Google Scholar 

  • Janson CH (2011) Reconciling rigor and range: observations, experiments, and quasi- experiments in field primatology. Int J Primatol 33:520–541

    Article  Google Scholar 

  • Janson CH, Byrne R (2007) What wild primates know about resources: opening up the black box. Anim Cogn 10:357–367

    Article  PubMed  Google Scholar 

  • Janson CH, Di Bitetti MS (1997) Experimental analysis of food detection in capuchin monkeys: effects of distance, travel speed, and resource size. Behav Ecol Sociobiol 41:17–24

    Article  Google Scholar 

  • Kaas JH, Huerta MF (1988) The subcortical visual system of primates. In: Steklis HD, Erwin J (eds) Comparative primate biology, vol 4. Alan RLiss, New York, pp 327–391

    Google Scholar 

  • Kass RE, Raftery AE (1995) Bayes factors and model uncertainty. J Am Statist Ass 90:773–795

    Article  Google Scholar 

  • Kruschke JK (2011) Bayesian assessment of null values via parameter estimation and model comparison. Prospect Psychol Sci 6:299–312

    Article  Google Scholar 

  • MacDonald SE (1994) Gorillas’ (Gorilla gorilla gorilla) spatial memory in a foraging task. J Comp Psychol 104:382–397

    Article  Google Scholar 

  • MacDonald SE, Agnes MM (1999) Orangutan (Pongo pygmaeus abelii) spatial memory and behavior in a foraging task. J Comp Psychol 113:213–217

    Article  Google Scholar 

  • MacDonald SE, Wilkie DM (1990) Yellow-nosed monkeys (Cercopithecus ascanius whitesidei) spatial memory in a simulated foraging experiment. J Comp Psychol 104:382–387

    Article  Google Scholar 

  • MacDonald SE, Pang JC, Gibeault S (1994) Marmoset (Callithrix jacchus jacchus) spatial memory in a foraging task: win-stay versus win-shift strategies. J Comp Psychol 108:328–334

    Article  PubMed  CAS  Google Scholar 

  • MacKinnon J (1974) The behaviour and ecology of wild orang-utans (Pongo pygmaeus). Anim Behav 22:3–74

    Article  Google Scholar 

  • MacLean EL, Matthews LJ, Hare BA, Nunn CL, Anderson RC, Aureli F, Brannon EM, Call J, Drea CM, Emery NJ, Haun DBM, Herrmann E, Jacobs LF, Platt ML, Rosati AG, Sandel AA, Schroepfer KK, Seed AM, Tan J, van Schaik CP, Wobber V (2012) How does cognition evolve? Phylogenetic comparative psychology. Anim Cogn 15:223–238

    Article  PubMed Central  PubMed  Google Scholar 

  • Marsh HL, Spetch ML, MacDonald SE (2011) Strategies in landmark use by orangutans and human children. Anim Cogn 14:487–502

    Article  PubMed  Google Scholar 

  • Martin RD (1990) Primate origins and evolution. Princeton University Press, New Jersey

    Google Scholar 

  • McDonald JH (2009) Handbook of biological statistics, 2nd edn. Sparky House Publishing, Baltimore

    Google Scholar 

  • Menzel EW (1973) Chimpanzee spatial memory organization. Science 182:943–945

    Article  PubMed  CAS  Google Scholar 

  • Normand E, Boesch C (2009) Sophisticated Euclidean maps in forest chimpanzees. Anim Behav 77:1195–1201

    Article  Google Scholar 

  • Noser RW, Byrne RW (2007) Mental maps in chacma baboons (Papio ursinus): using intergroup encounters as a natural experiment. Anim Cogn 10:331–347

    Article  PubMed  Google Scholar 

  • Noser RW, Byrne RW (2010) How do wild baboons (Papio ursinus) plan their routes? Travel among multiple high-quality food sources with inter-group competition. Anim Cogn 13:145–155

    Article  PubMed  Google Scholar 

  • Pariente G (1979) The role of vision in prosimian behavior. In: Doyle GA, Martin RD (eds) The study of prosimian behavior. Academic Press, New York, pp 411–459

    Google Scholar 

  • Platt ML, Brannon EM, Briese TL, French JA (1996) Differences in feeding ecology predict differences in performance between golden lion tamaris (Leontopithecus rosalia) and Wied’s marmosets (Callithrix kuhli) on spatial and visual memory tasks. Anim Learn Behav 24:384–393

    Article  Google Scholar 

  • Potì P, Bartolommei P, Saporiti M (2005) Landmark use by Cebus apella. Int J Primatol 26:921–948

    Article  Google Scholar 

  • Potì P, Kanngiesser R, Saporiti M, Amiconi A, Bläsing B, Call J (2010) Searching the middle- capuchins’ (Cebus apella) and bonobos’ (Pan paniscus) behavior during a spatial search task. J Exp Psychol Anim Behav Process 36:92–109

    Article  PubMed  Google Scholar 

  • Poucet B (1993) Spatial cognitive maps in animals: new hypotheses on their structure and neural mechanisms. Psychol Rev 100:163–182

    Article  PubMed  CAS  Google Scholar 

  • Rushmore J, Leonhardt SD, Drea CM (2012) Sight or scent: lemur sensory reliance in detecting food quality varies with feeding ecology. PLoS One 7:e41558

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Saj TL, Paterson JD, Sicotte P (2001) The conflict between vervet monkeys and farmers at the forest edge in Entebbe, Uganda. Afr J Ecol 39:195–199

    Article  Google Scholar 

  • Séguinot V, Maurer R, Etienne AS (1993) Dead reckoning in a small mammal: the evaluation of distance. J Comp Physiol A 173:103–113

    Article  PubMed  Google Scholar 

  • Shettleworth SJ (2010) Cognition, evolution, and behavior. Oxford University Press, New York

    Google Scholar 

  • Skinner JD, Smithers RHN (1990) The mammals of the southern African subregion. University of Pretoria, Pretoria

    Google Scholar 

  • Smith T, Rossie J (2006) Primate olfaction: anatomy and evolution. In: Brewer WJ, Castle D, Pantelis C (eds) Olfaction and the brain. Cambridge University Press, New York, pp 135–166

    Chapter  Google Scholar 

  • Sokal RR, Rohlf FJ (1981) Biometry. WH Freeman, New York

    Google Scholar 

  • Spetch ML, Kelly DM (2006) Comparative spatial cognition: processes in landmark- and surface-based place finding. In: Wasserman EA, Zentall TR (eds) Comparative cognition: experimental explorations of animal intelligence. Oxford University Press, New York, pp 210–228

    Google Scholar 

  • Sumner P, Mollon JD (2000) Catarrhine photopigments and optimized for detecting targets against a foliage background. J Exp Biol 203:1963–1986

    PubMed  CAS  Google Scholar 

  • Sutton JE, Olthof A, Roberts WA (2000) Landmark use by squirrel monkeys (Saimiri sciureus). Anim Lean Behav 28:28–42

    Article  Google Scholar 

  • Suzuki S, Augerinos G, Black AH (1980) Stimulus control of spatial behavior on the eight-arm maze in rats. Learn Motiv 11:1–18

    Article  Google Scholar 

  • Terborgh J (1983) Five new world primates. Princeton University Press, Princeton

    Google Scholar 

  • Valero A, Byrne RW (2007) Spider monkey ranging patterns in Mexican subtropical forest: do travel routes reflect planning? Anim Cogn 10:305–331

    Article  PubMed  Google Scholar 

  • Vallortigara G, Zanforlin M, Pasti G (1990) Geometric modules in animals’ spatial representations: a test with chicks (Gallus gallus domesticus). J Comp Psychol 104:248–254

    Article  PubMed  CAS  Google Scholar 

  • Vickers NJ (2000) Mechanisms of animal navigation in odor plumes. Biol Bull 198:203–212

    Article  PubMed  CAS  Google Scholar 

  • Waller D, Lippa Y (2007) Landmarks as beacons and associative cues: their role in route learning. Mem Cogn 35:910–924

    Article  Google Scholar 

  • Wang RF, Spelke ES (2002) Human spatial representation: insights from animals. Trends Cogn Sci 6:376–382

    Article  PubMed  Google Scholar 

  • Warburton K (1990) The use of local landmarks by foraging goldfish. Anim Behav 40:500–505

    Article  Google Scholar 

  • Wehner R, Raeber F (1979) Visual spatial memories in desert ants, Cataglyphis bicolor (Hymenoptera: Formicidae). Experientia 35:1569–1571

    Article  Google Scholar 

  • Wehner R, Srinivasan MV (1981) Searching behaviour of desert ants, genus Cataglyphis. J Comp Physiol A 142:315–338

    Article  Google Scholar 

  • Wehner R, Lehrer M, Harvey P (1996) Navigation. J Exp Biol 199:1–261

    Article  Google Scholar 

  • Wrangham RW, Waterman PG (1981) Feeding behaviour of vervet monkeys on Acacia tortilis and Acacia xanthophloea: with special reference to reproductive strategies and tannin production. J Anim Ecol 50:715–731

    Article  Google Scholar 

Download references

Acknowledgments

We thank the Uganda Wildlife Authority and the Uganda National Council for Science and Technology for permission to conduct this research, and methods were approved by the McGill University Animal Care committee. We are also grateful to Dennis Twinomugisha, Patrick Omeja, Lauren Chapman, Matovu Ponsiano, Maxine White, Jan Gogarten, and Jessica Rothman, who provided assistance both in and out of the field. Paul Garber provided valuable advice at the beginning of this study, and this manuscript was improved with helpful comments from Amanda Melin. Two anonymous reviewers improved the quality of this manuscript. Funding was provided by the Natural Sciences and Engineering Research Council of Canada.

Author information

Authors and Affiliations

  1. Department of Anthropology, University of California Santa Cruz, 1156 High Street, Santa Cruz, CA, 95064, USA

    Julie A. Teichroeb

  2. Department of Anthropology, McGill University, 855 Sherbrooke Street W., Montreal, QC, H3A 2T7, Canada

    Julie A. Teichroeb & Colin A. Chapman

  3. Wildlife Conservation Society, 2300 Southern Boulevard, Bronx, NY, 10460, USA

    Colin A. Chapman

Authors
  1. Julie A. Teichroeb
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Colin A. Chapman
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Julie A. Teichroeb.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Teichroeb, J.A., Chapman, C.A. Sensory information and associative cues used in food detection by wild vervet monkeys. Anim Cogn 17, 517–528 (2014). https://doi.org/10.1007/s10071-013-0683-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10071-013-0683-2

Keywords

Search

Navigation