Skip to main content

Advertisement

SpringerLink
Log in

The ecology of spatial memory in four lemur species

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

Abstract

Evolutionary theories suggest that ecology is a major factor shaping cognition in primates. However, there have been few systematic tests of spatial memory abilities involving multiple primate species. Here, we examine spatial memory skills in four strepsirrhine primates that vary in level of frugivory: ruffed lemurs (Varecia sp.), ring-tailed lemurs (Lemur catta), mongoose lemurs (Eulemur mongoz), and Coquerel’s sifakas (Propithecus coquereli). We compare these species across three studies targeting different aspects of spatial memory: recall after a long-delay, learning mechanisms supporting memory and recall of multiple locations in a complex environment. We find that ruffed lemurs, the most frugivorous species, consistently showed more robust spatial memory than the other species across tasks—especially in comparison with sifakas, the most folivorous species. We discuss these results in terms of the importance of considering both ecological and social factors as complementary explanations for the evolution of primate cognitive skills.

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
Fig. 4

Similar content being viewed by others

References

  • Anderson JR, Mitchell RW (1999) Macaques but not lemurs co-orient visually with humans. Folia Primatol 70:17–22

    Article  CAS  PubMed  Google Scholar 

  • Avian Brain Nomenclature Consortium (2005) Avian brains and a new understanding of vertebrate brain evolution. Nat Rev Neurosci 6:151–155

    Google Scholar 

  • Balda RP, Kamil AC (1989) A comparative study of cache recovery by three corvid species. Anim Behav 38:486–495

    Article  Google Scholar 

  • Barton RA (2006) Primate brain evolution: integrating comparative, neurophysiological, and ethological data. Evol Anthropol 15:224–236

    Article  Google Scholar 

  • Bednekoff PA, Balda RP, Kamil AC, Hile AG (1997) Long term memory in four seed-caching corvid species. Anim Behav 53:335–341

    Article  Google Scholar 

  • Bird CM, Burgess N (2008) The hippocampus and memory: insights from spatial processing. Nat Rev Neurosci 9:182

    Article  CAS  PubMed  Google Scholar 

  • Bolker BM, Brooks ME, Clark CJ, Geange SW, Poulsen JR, Stevens MHH, White JSS (2008) Generalized linear mixed models: a practical guide for ecology and evolution. Trends Ecol Evol 24:127–135

    Article  Google Scholar 

  • Bray J, Krupenye C, Hare B (2013) Ring-tailed lemurs (Lemur catta) exploit information about what others can see but not what they can hear. Anim Cogn. doi:10.1007/s10071-013-0705-0

    Google Scholar 

  • Britt A (2000) Diet and feeding behaviour of the black-and-white ruffed lemur (Varecia variegata variegata) in the Betampona Reserve, eastern Madagascar. Folia Primatol 71:133–141

    Article  CAS  PubMed  Google Scholar 

  • Buckner RL, Carroll DC (2007) Self-projection and the brain. Trends Cogn Sci 11(2):49–57

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Burgess N (2008) Spatial cognition and the brain. Ann NY Acad Sci 1124:77–97

    Article  PubMed  Google Scholar 

  • Byrne RW (1997) The technical intelligence hypothesis: an additional evolutionary stimulus to intelligence? In: Whiten A, Byrne RW (eds) Machiavellian intelligence II: extensions and evaluations. Cambridge University Press, Cambridge, pp 289–311

    Chapter  Google Scholar 

  • Byrne RW, Whiten AW (1988) Machiavellian intelligence: social expertise and the evolution of intellect in monkeys, apes, and humans. Clarendon Press, Oxford

    Google Scholar 

  • Campbell JL, Eisemann JH, Williams CV, Glenn KM (2000) Description of the gastrointestinal tract of five lemur species: propithecus tattersalli, Propithecus verreauxi coquereli, Varecia variegata, Hapalemur griseus, and Lemur catta. Am J Primatol 52:133–142

    Article  CAS  PubMed  Google Scholar 

  • Clutton-Brock TH, Harvey PH (1980) Primates, brains, and ecology. J Zool 190:309–323

    Article  Google Scholar 

  • Cuozzo FP, Yamashita N (2006) The impact of ecology on the teeth of extant lemurs: a review of dental adaptations, function, and life history. In: Sauther ML, Gould L (eds) Lemurs: ecology and adaptation. Springer, New York, pp 67–96

    Chapter  Google Scholar 

  • Curtis DJ (2004) Diet and nutrition in wild mongoose lemurs (Eulemur mongoz) and their implications for the evolution of female dominance and small group size in lemurs. Am J Phys Anthropol 124(3):234–247

    Article  PubMed  Google Scholar 

  • Curtis DJ, Zaramody A (1999) Social structure and seasonal variation in the behaviour of Eulemur mongoz. Folia Primatol 70(2):79–96

    Article  CAS  PubMed  Google Scholar 

  • Davachi L (2006) Item, context and relational episodic encoding in humans. Curr Opin Neurobiol 16:693–700

    Article  CAS  PubMed  Google Scholar 

  • de Waal FBM (1982) Chimpanzee politics: power and sex among apes. Harper & Row, New York

    Google Scholar 

  • Deaner RO, Barton RA, van Schaik CP (2003) Primate brains and life histories: renewing the connection. In: Kappeler PM, Pereira ME (eds) Primate life histories and socioecology. University of Chicago Press, Chicago, pp 233–265

    Google Scholar 

  • Dunbar RI (1998) The social brain hypothesis. Evol Anthr 6:178–190

    Article  Google Scholar 

  • Emery NJ, Clayton NS (2004) The mentality of crows: convergent evolution of intelligence in corvids and apes. Science 306:1903–1907

    Article  CAS  PubMed  Google Scholar 

  • Fichtel C, Kappeler PM (2010) Human universals and primate symplesiomorphies: establishing the lemur baseline. In: Kappeler PM, Silk JB (eds) Mind the gap: tracing the origins of human universals. Springer, New York, pp 395–428

  • Garamszegi LZ, Eens M (2004) The evolution of hippocampus volume and brain size in relation to food hoarding in birds. Ecol Lett 7:1216–1224

    Article  Google Scholar 

  • Genty E, Roeder JJ (2006) Can lemurs learn to deceive? A study in the black lemur. J Exp Psychol Anim B 32:196–200

    Article  Google Scholar 

  • Gibson KR (1986) Cognition, brain size and the extraction of embedded food resources. In: Else JG, Lee PC (eds) Primate ontogeny, cognition and social behaviour. Cambridge University Press, Cambridge, pp 93–105

  • Hampton RR, Hampstead BM, Murray EA (2004) Selective hippocampal damage impairs spatial memory in an open-field test in rhesus monkeys. Hippocampus 14:808–818

    Article  PubMed  Google Scholar 

  • Haun DBM, Nawroth C, Call J (2011) Great apes’ risk-taking strategies in a decision making task. PLoS One 6:e28801

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Healy SD, de Kort SR, Clayton NS (2005) The hippocampus, spatial memory, and food hoarding: a puzzle revisited. Trends Ecol Evol 20:17–22

    Article  PubMed  Google Scholar 

  • Heilbronner SH, Rosati AG, Stevens JR, Hare B, Hauser M (2008) A fruit in the hand or two in the bush? Divergent risk preferences in chimpanzees and bonobos. Biol Lett 4:246–249

    Article  PubMed Central  PubMed  Google Scholar 

  • Horvath JE, Weisrock DW, Embry SL, Fiorentino I, Balhoff JP, Kappeler P, Wray GA, Willard HF, Yoder AD (2008) Development and application of a phylogenomic toolkit: resolving the evolutionary history of Madagascar’s lemurs. Genome Res 18:489–499

    Article  CAS  PubMed Central  PubMed  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 

  • Jolly A (1966) Lemur social behavior and primate intelligence. Science 153:501–506

    Article  CAS  PubMed  Google Scholar 

  • Jones SM, Pearson J, DeWind NK, Paulsen D, Tenekedjieva A, Brannon EM (2013) Lemurs and macaques show similar numerical sensitivity. Anim Cogn. doi:10.1007/s10071-013-0682-3

    PubMed Central  Google Scholar 

  • Kamil AC, Balda RP, Olson DJ (1994) Performance of four seed-caching corvid species in the radial-arm maze analog. J Comp Psychol 108:385–393

    Article  CAS  PubMed  Google Scholar 

  • Krebs JR, Davies NB (1997) Behavioural ecology: an evolutionary approach, 4th edn. Blackwell Science, Oxford

    Google Scholar 

  • Krebs JR, Sherry DF, Healy SD, Perry H, Vaccarino AL (1989) Hippocampal specialization of food-storing birds. Proc Natl Acad Sci USA 86:1388–1392

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Languillea S, Blancb S, Blinc O et al (2012) The grey mouse lemur: a non-human primate model for aging studies. Ageing Res Rev 11:150–162

    Article  Google Scholar 

  • Lewis KP, Jaffe S, Brannon EM (2005) Analog number representation in mongoose lemurs (Eulemur mongoz): evidence from a search task. Anim Cogn 8:247–252

    Article  PubMed  Google Scholar 

  • Luehrs M, Dammhahn M, Kappeleler PM, Fichtel C (2009) Spatial memory in the grey mouse lemur (Microcebus murinus). Anim Cogn 12:599–609

    Article  Google Scholar 

  • MacLean EL, Merritt DJ, Brannon EM (2008) Social complexity predicts transitive reasoning in prosimian primates. Anim Behav 76:479–486

    Article  PubMed Central  PubMed  Google Scholar 

  • MacLean EL, Barrickman NL, Johnson EM, Wall CE (2009) Sociality, ecology, and relative brain size in lemurs. J Hum Evol 56(5):471–478

    Article  PubMed  Google Scholar 

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

    Article  PubMed Central  PubMed  Google Scholar 

  • MacLean EL, Mandalaywala TM, Brannon EM (2012b) Variance-sensitive choice in lemurs: constancy trumps quantity. Anim Cogn 15:15–25

    Article  PubMed Central  PubMed  Google Scholar 

  • MacLean E, Sandel A, Bray J, Oldenkamp R, Reddy R, Hare B (2013) Group size predicts social but not nonsocial cognition in lemurs. PLoS One 8:e66359

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Maguire EA, Burgess N, Donnett JG, Frackowiak RSJ, Frith CD, O’Keefe J (1998) Knowing where and getting there: a human navigation network. Science 280:921–924

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Merritt D, MacLean EL, Jaffe S, Brannon EM (2007) A comparative analysis of serial ordering in ring-tailed lemurs (Lemur catta). J Comp Psychol 12:363–371

    Article  Google Scholar 

  • Milton K (1981) Distribution patterns of tropical plant foods as an evolutionary stimulus to primate mental development. Am Anthropol 83(3):534–548

    Article  Google Scholar 

  • Mittermeier RA, Ganzhorn JU, Konstant WR, Glander K, Tattersall I, Groves CP, Rylands AB, Hapke A, Ratsimbazafy J, Mayor MI, Louis EE, Rumpler Y, Schwitzer C, Rasoloarison RM (2008) Lemur diversity in Madagascar. Int J Primatol 29:1607–1656

    Article  Google Scholar 

  • Morris RG, Garrud P, Rawlins JNP, O’Keefe J (1982) Place navigation impaired in rates with hippocampal lesions. Nature 297:681–683

    Article  CAS  PubMed  Google Scholar 

  • Murty VP, LaBar KS, Hamilton DA, Adcock RA (2011) Is all motivation good for learning: dissociable influences of approach and avoidance motivation in declarative memory. Learn Mem 18:712–717

    Article  PubMed Central  PubMed  Google Scholar 

  • Newcombe NS, Huttenlocher J (2006) Development of spatial cognition. In: Damon W, Lerner RM, Kuhn D, Siegler RS (eds) Handbook of child psychology, vol II. Cognition, perception, and language. Wiley, New York, pp 734–776

  • Newcombe NS, Huttenlocher J, Drummey A, Wiley JG (1998) The development of spatial location coding: place learning and dead reckoning in the second and third years. Cogn Dev 13:185–200

    Article  Google Scholar 

  • Packard MG (1996) Inactivation of hippocampus or caudate nucleus with lidocaine differentially affects expression of place and response learning. Neurobiol Learn Mem 65:65–72

    Article  CAS  PubMed  Google Scholar 

  • Packard MG (1999) Glutamate infused posttraining into the hippocampus or caudate-putamen differentially strengthens place and response learning. Proc Natl Acad Sci USA 96:12881–12886

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Packard MG (2009) Exhumed from thought: basal ganglia and response learning in the plus-maze. Behav Brain Res 199:24–31

    Article  PubMed  Google Scholar 

  • Packard MG, Goodman J (2013) Factors that influence the relative use of multiple memory systems. Hippocampus 23:1044–1052

    Google Scholar 

  • Parker ST, Gibson KR (1997) Object manipulation, tool use and sensorimotor intelligence as feeding adaptations in Cebus monkeys and great apes. J Hum Evol 6:623–641

    Article  Google Scholar 

  • Picq J-L (1993) Radial maze performance in young and aged grey mouse lemurs (Microcebus murinus). Primates 34:223–226

    Article  Google Scholar 

  • Picq J (2007) Aging affects executive functions and memory in mouse lemur primates. Exp Gerontol 42:223–232

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Poldrack RA, Packard MG (2003) Competition among multiple memory systems: converging evidence from animal and human brain studies. Neuropsychologia 41:245–251

    Article  PubMed  Google Scholar 

  • Poldrack RA, Clark MA, Pare-Blagoev EJ, Shohamy D, Creso Moyan J, Myers C, Gluck MA (2001) Interactive memory systems in the human brain. Nature 414:546

    Article  CAS  PubMed  Google Scholar 

  • Richard AF (1977) The feeding behaviour of Propithecus verreauxi. In: Clutton-Brock T (ed) Primate ecology: studies of feeding and ranging behaviour in lemurs, monkeys and apes. Academic Press, London, pp 71–96

    Google Scholar 

  • Richard AF, Dewar RE (1991) Lemur ecology. Ann Rev Ecol Syst 22:145–175

    Article  Google Scholar 

  • Rosati AG, Hare B (2012a) Chimpanzees and bonobos exhibit divergent spatial memory development. Dev Sci 15:840–853

    Article  PubMed  Google Scholar 

  • Rosati AG, Hare B (2012b) Decision-making across social contexts: competition increases preferences for risk in chimpanzees and bonobos. Anim Behav 84:869–879

    Article  Google Scholar 

  • Rosati AG, Hare B (2013) Chimpanzees and bonobos exhibit emotional responses to decision outcomes. PLoS ONE 8:e63058

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Rosati AG, Stevens JR, Hauser MD (2006) The effect of handling time on temporal discounting in two New World primates. Anim Behav 71:1379–1387

    Article  Google Scholar 

  • Rosati AG, Stevens JR, Hare B, Hauser M (2007) The evolutionary origins of human patience: temporal preferences in chimpanzees, bonobos, and human adults. Curr Biol 17:1663–1668

    Article  CAS  PubMed  Google Scholar 

  • Ruiz A, Gomes JC, Roeder JJ, Byrne RW (2009) Gaze following and gaze priming in lemurs. Anim Cogn 12:427–434

    Article  PubMed  Google Scholar 

  • Sandel AA, MacLean EL, Hare B (2011) Evidence from four lemur species that ring-tailed lemur social cognition converges with that of haplorhine primates. Anim Behav 81:925–931

    Article  Google Scholar 

  • Santos LR, Barnes JL, Mahajan N (2005) Expectations about numerical events in four lemurs species (Eulemur fulvus, Eulemur mongoz, Lemur catta and Varecia rubra). Anim Cogn 8:253–262

    Article  PubMed  Google Scholar 

  • Sauther ML, Sussman RW, Gould L (1999) The socioecology of the ringtailed lemur: thirty-five years of research. Evol Anthropol 8(4):120–132

    Article  Google Scholar 

  • Shepherd SV, Platt ML (2008) Spontaneous social orienting and gaze following in ringtailed lemurs (Lemur catta). Anim Cogn 11:13–20

    Article  PubMed  Google Scholar 

  • Sherry DF (2006) Neuroecology. Annu Rev Psychol 57:167–197

    Article  PubMed  Google Scholar 

  • Sherry DF, Schacter DL (1987) The evolution of multiple memory systems. Psychol Rev 94:439–454

    Article  Google Scholar 

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

    Google Scholar 

  • Shohamy D, Adcock RA (2010) Dopamine and adaptive memory. Trends Cogn Sci 14:464–472

    Article  CAS  PubMed  Google Scholar 

  • Sluzenski J, Newcombe NS, Satlow E (2004) Knowing where things are in the second year of life: implications for hippocampal development. J Cogn Neurosci 16:1443–1451

    Article  PubMed  Google Scholar 

  • Stevens JR, Muhlhoff N (2012) Intertemporal choice in lemurs. Behav Proc 89:121–127

    Article  Google Scholar 

  • Stevens JR, Hallinan EV, Hauser MD (2005a) The ecology and evolution of patience in two New World monkeys. Bio Lett 1:223–226

    Article  Google Scholar 

  • Stevens JR, Rosati AG, Ross K, Hauser MD (2005b) Will travel for food: spatial discounting in two New World monkeys. Curr Biol 15:1855–1860

    Article  CAS  PubMed  Google Scholar 

  • R Development Core Team (2011) A language and environment for statistical computing. http://www.R-project.org

  • Tomasello M, Call J (2011) Methodological challenges in the study of primate cognition. Science 334:1227–1228

    Article  CAS  PubMed  Google Scholar 

  • Vasey N (2005) New developments in the behavioral ecology and conservation of ruffed lemurs (Varecia). Am J Primatol 66(1):1–6

    Article  PubMed  Google Scholar 

  • Yoder AD, Cartmill M, Ruvolo M, Smith K, Vilgalys R (1996) Ancient single origin for Malagasy primates. Proc Natl Acad Sci USA 93:5122–5126

    Article  CAS  PubMed Central  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Emma Blumstein, Joel Bray, Mary Danbro, Caroline Drucker, Korrina Duffy, Joseph Feldblum, Ben Finkel, Leah Kaiser, Sandeep Prasanna, Courtnea Rainey, Nate Rollins, and Kara Schroepfer-Walker with assistance in conducting the studies, and Taylor Jones for assistance in coding. At the Duke Lemur Center, we thank Sarah Zehr and David Brewer for their assistance. This research was supported by a Duke University Undergraduate Research grant to K.R. This is Duke Lemur Center publication #1263.

Author information

Authors and Affiliations

  1. Department of Psychology, Yale University, New Haven, CT, USA

    Alexandra G. Rosati

  2. Department of Evolutionary Anthropology, Duke University, Durham, NC, USA

    Kerri Rodriguez & Brian Hare

  3. Center for Cognitive Neuroscience, Duke University, Durham, NC, USA

    Brian Hare

Authors
  1. Alexandra G. Rosati
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kerri Rodriguez
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Brian Hare
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Alexandra G. Rosati.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 243 kb)

Test trial in Study 1 (memory after a one-week delay). The mongoose lemur is centered at the starting position by Experimenter 2 (E2) using a small piece of, while E1 baits the food cups. Once the baiting process is complete, E2 says start and removes the centering food. Here, the lemur chooses the correct (baited) cup. In the initial introductory session one week previously, lemurs could self-correct their choice following incorrect responses, to ensure equal experience with the correct location. In the test session one week later (shown here), lemurs could not self-correct (MOV 6738 kb)

Learning and probe trial in Study 2 (memory mechanisms). In the learning trial, the sifaka is centered at the normal staring position by Experimenter 2 (E2) using a small piece of food, while E1 baits the cups. As in Study 1, the lemur can self-correct following incorrect choices in learning trials. Here, the sifakas correctly chooses the baited side. In the probe trial, the sifakas begins the trial from the flipped orientation, and E1 baits both locations. Here, the sifakas makes a habit-based response (turning right) rather than a spatial response (toward the previously rewarded spatial location). E1 removes the food from the alternative location following the choice (MOV 10113 kb)

Search phase in Study 3 (memory for multiple locations). The ruffed lemur enters the room and searches at four of the eight landmarks. In the previous exposure phase, four test locations were baited with visible food, whereas the four control locations were empty. In the search phase shown here, all locations are baited with food, which are hidden by a lid covering the food boxes. Here, the lemur first searches at two control locations, and then at two test locations (MOV 38046 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Rosati, A.G., Rodriguez, K. & Hare, B. The ecology of spatial memory in four lemur species. Anim Cogn 17, 947–961 (2014). https://doi.org/10.1007/s10071-014-0727-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10071-014-0727-2

Keywords

Search

Navigation