Skip to main content
SpringerLink
Log in

Social inhibitory control in five lemur species

  • Original Article
  • Published:
Primates Aims and scope Submit manuscript

Abstract

We tested five lemur species—ring-tailed lemurs, ruffed lemurs, mongoose lemurs, black lemurs, and Coquerel’s sifakas—(N = 52) in an experiment that evaluated skills for inhibitory control in a social context. First, two human experimenters presented identical food rewards; the “generous” experimenter allowed the subject to eat from her hand, whereas the “competitive” experimenter always withheld the reward. Lemurs quickly learned to approach the generous experimenter and avoid the competitive one. In the inhibition test phase, we endowed the competitive experimenter with a more valuable food reward but the competitive experimenter continued to withhold food from the subject. Thus, lemurs were required to inhibit approaching the more desirable reward in favor of the lesser but obtainable reward presented by the generous experimenter. In test trials, lemurs’ tendency to approach the competitive experimenter increased from the reputation phase, demonstrating sensitivity to the experimental manipulation. However, subjects approached the larger reward less frequently in test trials compared with pretest food-preference trials, evidencing some capacity for inhibitory control in this context. Despite differences in sociality and ecology, the five lemur species did not differ in this ability. Although the study did not uncover species differences, this experimental task may provide a useful measure of social inhibition in broader comparative studies.

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

  • Albiach-Serrano A, Guillen-Salazar F, Call J (2007) Mangabeys (Cercocebus torquatus lunulatus) solve the reverse contingency task without a modified procedure. Anim Cogn 10:387–396

    Article  PubMed  Google Scholar 

  • Altman DG (1991) Practical statistics for medical research. Chapman and Hall, London

    Google Scholar 

  • Amici F, Aureli F, Call J (2008) Fission–fusion dynamics, behavioral flexibility, and inhibitory control in primates. Curr Biol 18:1415–1419

    Article  CAS  PubMed  Google Scholar 

  • Anderson JR, Awazu S, Fujita K (2004) Squirrel monkeys (Saimiri sciureus) choose smaller food arrays: long-term retention, choice with nonpreferred food, and transposition. J Comp Psychol 118:58–64

    Article  PubMed  Google Scholar 

  • Anderson JR, Kuroshima H, Fujita K (2010) Delay of gratification in capuchin monkeys (Cebus apella) and squirrel monkeys (Saimiri sciureus). J Comp Psychol 124:205–210

    Article  PubMed  Google Scholar 

  • Auersperg A, Laumer I, Bugnyar T (2013) Goffin cockatoos wait for qualitative and quantitative gains but prefer ‘better’to ‘more’. Biol Letters 9:20121092

    Article  CAS  Google Scholar 

  • Baden AL, Wright PC, Louis EE Jr, Bradley BJ (2013) Communal nesting, kinship, and maternal success in a social primate. Behav Ecol Sociobiol 67:1939–1950

    Article  Google Scholar 

  • Beran MJ, Evans TA (2009) Delay of gratification by chimpanzees (Pan troglodytes) in working and waiting situations. Behav Process 80:177–181

    Article  Google Scholar 

  • Bond AB, Kamil AC, Balda RP (2007) Serial reversal learning and the evolution of behavioral flexibility in three species of North American corvids (Gymnorhinus cyanocephalus, Nucifraga columbiana, Aphelocoma californica). J Comp Psychol 121:372–379

    Article  PubMed  Google Scholar 

  • Boogert NJ, Anderson RC, Peters S, Searcy WA, Nowicki S (2011) Song repertoire size in male song sparrows correlates with detour reaching, but not with other cognitive measures. Anim Behav 81:1209–1216

    Article  Google Scholar 

  • Boysen ST, Berntson GG (1995) Responses to quantity: perceptual versus cognitive mechanisms in chimpanzees (Pan troglodytes). J Exp Psychol Anim B 21:82–86

    Article  CAS  Google Scholar 

  • Bray EE, MacLean EL, Hare BA (2014a) Context specificity of inhibitory control in dogs. Anim Cogn 17:15–31

    Article  PubMed Central  PubMed  Google Scholar 

  • Bray J, Krupenye C, Hare B (2014b) Ring-tailed lemurs (Lemur catta) exploit information about what others can see but not what they can hear. Anim Cogn 17:735–744

    Article  PubMed  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 

  • Chudasama Y, Kralik JD, Murray EA (2007) Rhesus monkeys with orbital prefrontal cortex lesions can learn to inhibit prepotent responses in the reversed reward contingency task. Cereb Cortex 17:1154–1159

    Article  CAS  PubMed  Google Scholar 

  • Colquhoun IC (1998) Cathemeral behavior of Eulemur macaco macaco at Ambato Massif, Madagascar. Folia Primatol 69:22–34

    Article  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 Anthropo 124:234–247

    Article  Google Scholar 

  • Danisman E, Bshary R, Bergmüller R (2010) Do cleaner fish learn to feed against their preference in a reverse reward contingency task? Anim Cogn 13:41–49

    Article  PubMed  Google Scholar 

  • Duckworth AL, Kern ML (2011) A meta-analysis of the convergent validity of self-control measures. J Res Pers 45:259–268

    Article  PubMed Central  PubMed  Google Scholar 

  • Dufour V, Pelé M, Sterck EHM, Thierry B (2007) Chimpanzee (Pan troglodytes) anticipation of food return: coping with waiting time in an exchange task. J Comp Psychol 121:145–155

    Article  CAS  PubMed  Google Scholar 

  • Evans TA, Beran MJ (2007) Delay of gratification and delay maintenance by rhesus macaques (Macaca mulatta). J Gen Psychol 134:199–216

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Genty E, Roeder J (2007) Transfer of self-control in black (Eulemur macaco) and brown (Eulemur fulvus) lemurs: choice of a less preferred food item under a reverse-reward contingency. J Comp Psychol 121:354–362

    Article  PubMed  Google Scholar 

  • Genty E, Palmier C, Roeder J (2004) Learning to suppress responses to the larger of two rewards in two species of lemurs, Eulemur fulvus and E. macaco. Anim Behav 67:925–932

    Article  Google Scholar 

  • Genty E, Foltz J, Roeder J (2008) Can brown lemurs (Eulemur fulvus) learn to deceive a human competitor? Anim Cogn 11:255–266

    Article  PubMed  Google Scholar 

  • Genty E, Chung PCS, Roeder J (2011) Testing brown lemurs (Eulemur fulvus) on the reverse-reward contingency task without a modified procedure. Behav Process 86:133–137

    Article  Google Scholar 

  • Gould L (2007) Lemur catta ecology: what we know and what we need to know. In: Gould L, Sauther ML (eds) Lemurs: ecology and adaptation. Springer, New York, pp 255–274

    Google Scholar 

  • Hare B (2001) Can competitive paradigms increase the validity of experiments on primate social cognition? Anim Cogn 4:269–280

    Article  CAS  PubMed  Google Scholar 

  • Hayden BY, Platt ML (2007) Animal cognition: great apes wait for grapes. Curr Biol 17:R922–R923

    Article  CAS  PubMed  Google Scholar 

  • Herrmann E, Keupp S, Hare B, Vaish A, Tomasello M (2013) Direct and indirect reputation formation in nonhuman great apes (Pan paniscus, Pan troglodytes, Gorilla gorilla, Pongo pygmaeus) and human children (Homo sapiens). J Comp Psychol 127:63–75

    Article  PubMed  Google Scholar 

  • Hinde RA (1970) Animal behaviour: a synthesis of ethology and comparative psychology. McGraw-Hill Inc, USA

    Google Scholar 

  • Hochberg Y, Benjamini Y (1990) More powerful procedures for multiple significance testing. Stat Med 9:811–818

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Kralik JD (2005) Inhibitory control and response selection in problem solving: how cotton-top tamarins (Saguinus oedipus) overcome a bias for selecting the larger quantity of food. J Comp Psychol 119:78–89

    Article  PubMed  Google Scholar 

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

    Article  PubMed Central  PubMed  Google Scholar 

  • MacLean EL, Matthews L, Hare B, Nunn C, Anderson R, Aureli F, Brannon E, Call J, Drea C, Emery N et al (2012) How does cognition evolve? Phylogenetic comparative psychology. Anim Cogn 15:223–238

    Article  PubMed Central  PubMed  Google Scholar 

  • MacLean EL, Sandel AA, Bray J, Oldenkamp R, Reddy RB, Hare B (2013) Group size predicts social, but not nonsocial cognition in lemurs. PLoS One 8:0066359

    Article  Google Scholar 

  • MacLean EL, Hare B, Nunn CL, Addessi E, Amici F, Anderson RC, Aureli F, Baker JM, Bania AE, Barnard AM et al (2014) The evolution of self-control. P Natl Acad Sci USA 111:E2140–E2148

    Article  CAS  Google Scholar 

  • Malenky RK, Wrangham RW (1994) A quantitative comparison of terrestrial herbaceous food consumption by Pan paniscus in the Lomako Forest, Zaire, and Pan troglodytes in the Kibale Forest, Uganda. Am J Primatol 32:1–12

    Article  Google Scholar 

  • Mischel W, Shoda Y, Rodriguez ML (1989) Delay of gratification in children. Science 244:933–938

    Article  CAS  PubMed  Google Scholar 

  • Moffitt TE, Arseneault L, Belsky D, Dickson N, Hancox RJ, Harrington H, Houts R, Poulton R, Roberts BW, Ross S et al (2011) A gradient of childhood self-control predicts health, wealth, and public safety. Proc Natl Acad Sci USA 108:2693–2698

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Murray EA, Kralik JD, Wise SP (2005) Learning to inhibit prepotent responses: successful performance by rhesus macaques (Macaca mulatta) on the reversed-contingency task. Anim Behav 69:991–998

    Article  Google Scholar 

  • Paglieri F, Focaroli V, Bramlett J, Tierno V, McIntyre JM, Addessi E, Evans TA, Beran MJ (2013) The hybrid delay task: can capuchin monkeys (Cebus apella) sustain a delay after an initial choice to do so? Behav Process 94:45–54

    Article  Google Scholar 

  • Pelé M, Dufour V, Micheletta J, Thierry B (2010) Long-tailed macaques display unexpected waiting abilities in exchange tasks. Anim Cogn 13:263–271

    Article  PubMed  Google Scholar 

  • Pelé M, Micheletta J, Uhlrich P, Thierry B, Dufour V (2011) Delay maintenance in Tonkean macaques (Macaca tonkeana) and brown capuchin monkeys (Cebus apella). Int J Primatol 32:149–166

    Article  Google Scholar 

  • Rice WR, Gaines SD (1994) Extending nondirectional heterogeneity tests to evaluate simply ordered alternative hypotheses. Proc Natl Acad Sci USA 91:225–226

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Richard AF (1978) Behavioral variation: case study of a Malagasy lemur. Associated University Press, London

    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, Hare B, Hauser MD (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 

  • Rosati AG, Rodriguez K, Hare B (2014) The ecology of spatial memory in four lemur species. Anim Cogn 17:947–961

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Santos LR, Ericson BN, Hauser MD (1999) Constraints on problem solving and inhibition: object retrieval in cotton-top tamarins (Saguinus oedipus Oedipus). J Comp Psychol 113:186–193

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Silberberg A, Fujita K (1996) Pointing at smaller food amounts in an analogue of Boysen and Berntson’s (1995) procedure. J Exp Anal Behav 66:143–147

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Stevens JR, Rosati AG, Heilbronner SR, Mühlhoff N (2011) Waiting for grapes: expectancy and delayed gratification in bonobos. Int J Comp Psychol 24:99–111

    Google Scholar 

  • Subiaul F, Vonk J, Okamoto-Barth S, Barth J (2008) Do chimpanzees learn reputation by observation? Evidence from direct and indirect experience with generous and selfish strangers. Anim Cogn 11:611–623

    Article  PubMed  Google Scholar 

  • Tomasello M, Call J (1997) Primate cognition. Oxford University Press, New York

    Google Scholar 

  • Tsukayama E, Duckworth AL, Kim B (2012) Resisting everything except temptation: evidence and an explanation for domain-specific impulsivity. Eur J Personal 26:318–334

    Article  Google Scholar 

  • Uher J, Call J (2008) How the great apes (Pan troglodytes, Pongo pygmaeus, Pan paniscus, Gorilla gorilla) perform on the reversed reward contingency task II: transfer to new quantities, long-term retention, and the impact of quantity ratios. J Comp Psychol 122:204–212

    Article  PubMed  Google Scholar 

  • Vasey N (2007a) The breeding system of wild red ruffed lemurs (Varecia rubra): a preliminary report. Primates 48:41–54

    Article  PubMed  Google Scholar 

  • Vasey N (2007b) Impact of seasonality and reproduction on social structure, ranging patterns, and fission–fusion social organization in red ruffed lemurs. In: Gould L, Sauther ML (eds) Lemurs: ecology and adaptation. Springer, New York, pp 275–304

    Google Scholar 

  • Vick S-J, Bovet D, Anderson JR (2010) How do African grey parrots (Psittacus erithacus) perform on a delay of gratification task? Anim Cogn 13:351–358

    Article  PubMed  Google Scholar 

  • Vlamings PHJM, Uher J, Call J (2006) How the great apes (Pan troglodytes, Pongo pygmaeus, Pan paniscus, and Gorilla gorilla) perform on the reversed contingency task: the effects of food quantity and food visibility. J Exp Psychol Anim B 32:60–70

    Article  Google Scholar 

  • Vlamings PHJM, Hare B, Call J (2010) Reaching around barriers: the performance of the great apes and 3 to 5-year-old children. Anim Cogn 13:273–285

    Article  PubMed Central  PubMed  Google Scholar 

  • Wobber V, Hare B (2009) Testing the social dog hypothesis: are dogs also more skilled than chimpanzees in non-communicative social tasks? Behav Process 81:423–428

    Article  Google Scholar 

  • Wobber V, Wrangham R, Hare B (2010) Bonobos exhibit delayed development of social behavior and cognition relative to chimpanzees. Curr Biol 20:226–230

    Article  CAS  PubMed  Google Scholar 

  • Wobber V, Herrmann E, Hare B, Wrangham R, Tomasello M (2014) Differences in the early cognitive development of children and great apes. Dev Psychobiol 56:547–573

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

We thank the staff at the Duke Lemur Center, especially Dr. Sarah Zehr and David Brewer, without whom this project would not have been possible. We also thank Camila Caceres, Jesse St. Clair, Alex Lourie, and Isabel Bernstein for their help with data collection, and Laura Lewis for her help with coding. We thank Jeff Stevens and three anonymous reviewers for their helpful feedback on earlier versions of this manuscript. This research was supported by the National Science Foundation (Grant BCS-10-25172), the Howard Hughes Research Fellows program, and the Duke Undergraduate Research Support Office.

Author information

Authors and Affiliations

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

    Rachna B. Reddy, Evan L. MacLean & Brian Hare

  2. Department of Anthropology, University of Michigan, 101 West Hall, 1085 S. University Ave., Ann Arbor, MI, 48104, USA

    Rachna B. Reddy & Aaron A. Sandel

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

    Brian Hare

Authors
  1. Rachna B. Reddy
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Evan L. MacLean
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Aaron A. Sandel
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Brian Hare
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Rachna B. Reddy.

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Reddy, R.B., MacLean, E.L., Sandel, A.A. et al. Social inhibitory control in five lemur species. Primates 56, 241–252 (2015). https://doi.org/10.1007/s10329-015-0467-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10329-015-0467-1

Keywords

Search

Navigation