Abstract
The ability of an animal to integrate and retain spatial information of resources often depends on the spatial memory and the speed at which this memory crystallizes. These become especially important once foragers reach their target area. However, very little is known about how wild common marmosets encode spatial information when feeding rewards are near to each other in a small-scale space. With this in mind, we performed field experiments to test foraging decisions related to a small-scale space setting. Specifically, we tested the (i) short- and (ii) long-term spatial memory, as well as (iii) the ability to remember the spatial location of resources after a single visit (one-trial spatial learning). The study was conducted with four groups of wild common marmosets (Callithrix jacchus) living in a semiarid Caatinga environment. We observed that individuals were able to retain spatial information of food sources on both a short- and long-term basis and to learn the spatial location of these resources after a single visit. We suggest that such abilities during foraging can improve the search for scattered resources with fluctuations of food availability. Presumably, this would be particularly advantageous in Caatinga, with its vegetation exhibiting asynchronous phenological patterns. Altogether, our results demonstrate that common marmosets employ all three studied spatial cognitive abilities to improve their food search and consumption.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Abreu F, De la Fuente MFC, Schiel N, Souto A (2016) Feeding ecology and behavioral adjustments: flexibility of a small neotropical primate (Callithrix jacchus) to survive in a semiarid environment. Mammal Res 61:221–229. https://doi.org/10.1007/s13364-016-0262-4
Abreu F, Souto A, Bonci DMO, Montavani V, Pessoa DMA, Schiel N (2019) Detection of insect prey by wild common marmosets: the effect of color vision. Am J Primatol. https://doi.org/10.1002/ajp.22963
Albuquerque UP, Araújo EDL, El-Deir ACA et al (2012) Caatinga revisited: ecology and conservation of an important seasonal dry forest. Sci World J. https://doi.org/10.1100/2012/205182
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. https://doi.org/10.1016/0023-9690(88)90004-5
Araújo EDL, Castro CC, Albuquerque UP (2007) Dynamics of Brazilian Caatinga—a review concerning the plants, environment and people. Funct Ecosyst Communities 1:15–28
Baayen RH, Davidson DJ, Bates DM (2008) Mixed-effects modeling with crossed random effects for subjects and items. J Mem Lang 59:390–412. https://doi.org/10.1016/j.jml.2007.12.005
Bailey C, Bartsch D, Kandel E (1996) Toward a molecular definition of long-term memory storage. Proc Natl Acad Sci USA 93:13445–13452
Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48. https://doi.org/10.18637/jss.v067.i01
Bicca-Marques JC, Garber PA (2005) Use of social and ecological information in tamarin foraging decisions. Int J Primatol 26:1321–1344. https://doi.org/10.1007/s10764-005-8855-9
Bourjade M, Thierry B, Call J, Dufour V (2012) Are monkeys able to plan for future exchange? Anim Cogn 15:783–795. https://doi.org/10.1007/s10071-012-0502-1
Corlett RT (2011) How to be a frugivore (in a changing world). Acta Oecol 37:674–681. https://doi.org/10.1016/j.actao.2011.01.005
Crystal JD (2010) Episodic-like memory in animals. Behav Brain Res 215:235–243. https://doi.org/10.1016/j.bbr.2010.03.005
da Silva PO, Menino GCO, Reys P, Sá JL, Soares MP, Silva FG (2019) Phenology of Anacardium occidentale (Anacardiaceae) and relationship with climatic factors. Floresta 49:69–78. https://doi.org/10.5380/rf.v49i1.56310
De la Fuente MF, Schiel N, Bicca-Marques JC, Caselli CB, Souto A, Garber PA (2019) Balancing contest competition, scramble competition, and social tolerance at feeding sites in wild common marmosets (Callithrix jacchus). Am J Primatol. https://doi.org/10.1002/ajp.22964
De la Fuente MFC, Souto A, Sampaio MB, Schiel N (2014) Behavioral adjustments by a small neotropical primate (Callithrix jacchus) in a semiarid caatinga environment. Sci World J. https://doi.org/10.1155/2014/326524
DeCasien AR, Williams SA, Higham JP (2017) Primate brain size is predicted by diet but not sociality. Nat Ecol Evol 1:1–7. https://doi.org/10.1038/s41559-017-0112
Dolins FL (2009) Captive cotton-top tamarins’ (Saguinus oedipus oedipus) use of landmarks to localize hidden food items. Am J Primatol 71:316–323. https://doi.org/10.1002/ajp.20654
Easton A, Parker K, Derrington AM, Parker A (2003) Behaviour of marmoset monkeys in a T-maze: comparison with rats and macaque monkeys on a spatial delayed non-match to sample task. Exp Brain Res 150:114–116. https://doi.org/10.1007/s00221-003-1409-5
Fagan WF, Lewis MA, Auger-Méthé M, Avgar T, Benhamou S, Breed G, LaDage L, Schlägel UE, Tang W, Papastamatiou YP, Forester J, Mueller T (2013) Spatial memory and animal movement. Ecol Lett 16:1316–1329. https://doi.org/10.1111/ele.12165
Francisco TM, Couto DR, Zanuncio JC, Serrão JE, Silva IDO, Boere V (2014) Vegetable exudates as food for Callithrix spp. (Callitrichidae): exploratory patterns. PLoS ONE 9:1–7. https://doi.org/10.1371/journal.pone.0112321
Garber PA (2000) The ecology of group movement: evidence for the use of spatial, temporal, and social information in some primate foragers. In: Boinski S, Garber PA (eds) On the move. How and why animals travel in groups, Chicago. University of Chicago Press, Chicago, pp 261–298
Garber PA, Caselli CB, McKenney AC, Abreu F, De la Fuente MFC, Araújo A, Arruda MDF, Souto A, Schiel N, Bicca-Marques JC (2019) Trait variation and trait stability in common marmosets (Callithrix jacchus) inhabiting ecologically distinct habitats in northeastern Brazil. Am J Primatol. https://doi.org/10.1002/ajp.23018
Garber PA, Dolins F (1996) Testing learning paradigms in the field. In: Norconk MA, Rosenberger AL, Garber PA (eds) Adaptive radiations of neotropical primates. Springer US, Boston, pp 201–216
Garber PA, Dolins FL (2010) Examining spatial cognitive strategies in small-scale space and large-scale space in tamarin monkeys. In: Dolins FL, Mitchell RW (eds) Spatial cognition, spatial perception: mapping the self and space, 1st edn. Cambridge University Press, Cambridge, p 581
Garber PA, Dolins FL (2014) Primate spatial strategies and cognition: introduction to this special issue. Am J Primatol 76:393–398. https://doi.org/10.1002/ajp.22257
Garber PA, Paciulli LM (1997) Experimental field study of spatial memory and learning in wild capuchin monkeys (Cebus capucinus). Folia Primatol 68:236–253. https://doi.org/10.1159/000157250
Gomes DF, Bicca-Marques JCJC (2012) Capuchin monkeys (Cebus nigritus) use spatial and visual information during within-patch foraging. Am J Primatol 74:58–67. https://doi.org/10.1002/ajp.21009
Gomes VGN, Meiado MV, Quirino ZGM, de Araujo HFP, Machado IC (2017) Synchronous fruiting and common seed dispersers of two endemic columnar cacti in the Caatinga, a dry forest in Brazil. Plant Ecol 218:1325–1338. https://doi.org/10.1007/s11258-017-0771-5
Gunhold T, Massen JJM, Schiel N, Souto A, Bugnyar T (2014) Memory, transmission and persistence of alternative foraging techniques in wild common marmosets. Anim Behav 91:79–91. https://doi.org/10.1016/j.anbehav.2014.02.023
Hampton RR, Hampstead BM, Murray EA (2005) Rhesus monkeys (Macaca mulatta) demonstrate robust memory for what and where, but not when, in an open-field test of memory. Learn Motiv 36:245–259. https://doi.org/10.1016/j.lmot.2005.02.004
Harlow HF (1949) The formation of learning sets. Psychol Rev 56:51–65
Hladik CM (1977) Chimpanzees of Gabon and chimpanzees of Gombe: some comparative data on the diet. In: Clutton-Brock TH (ed) Primate ecology: studies of feeding and ranging behavior in lemurs, monkey and apes. Academic Press, London, pp 81–501
Hopkins ME (2016) Mantled howler monkey spatial foraging decisions reflect spatial and temporal knowledge of resource distributions. Anim Cogn 19:387–403. https://doi.org/10.1007/s10071-015-0941-6
Izar P, Verderane MP, Peternelli-dos-Santos L, Mendonça-Furtado O, Presotto A, Tokuda M, Visalberghi E, Fragaszy D (2012) Flexible and conservative features of social systems in tufted capuchin monkeys: comparing the socioecology of Sapajus libidinosus and Sapajus nigritus. Am J Primatol 74:315–331. https://doi.org/10.1002/ajp.20968
Janmaat KRL, Chapman CA, Meijer R, Zuberbühler K (2012) The use of fruiting synchrony by foraging mangabey monkeys: a “simple tool” to find fruit. Anim Cogn 15:83–96. https://doi.org/10.1007/s10071-011-0435-0
Janmaat KRL, Ban SD, Boesch C (2013) Chimpanzees use long-term spatial memory to monitor large fruit trees and remember feeding experiences across seasons. Anim Behav 86:1183–1205. https://doi.org/10.1016/j.anbehav.2013.09.021
Janmaat KRL, Boesch C, Byrne R, Chapman CA, Bi ZBG, Head JS, Robbins MM, Wrangham RW, Polansky L (2016) Spatio-temporal complexity of chimpanzee food: How cognitive adaptations can counteract the ephemeral nature of ripe fruit. Am J Primatol 78:626–645. https://doi.org/10.1002/ajp.22527
Kushwaha CP, Tripathi SK, Tripathi BD, Singh KP (2011) Patterns of tree phenological diversity in dry tropics. Acta Ecol Sin 31:179–185. https://doi.org/10.1016/j.chnaes.2011.04.003
Lacreuse A, Kim CB, Rosene DL, Killiany RJ, Moss MB, Moore TL, Chennareddi L, Herndon JG (2005) Sex, age, and training modulate spatial memory in the rhesus monkey (Macaca mulatta). Behav Neurosci 119:118–126. https://doi.org/10.1037/0735-7044.119.1.118
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. https://doi.org/10.1037/0735-7036.108.4.328
MacDonald SE, Spetch ML, Kelly DM, Cheng K (2004) Strategies in landmark use by children, adults, and marmoset monkeys. Learn Motiv 35:322–347. https://doi.org/10.1016/j.lmot.2004.03.002
Martin P, Bateson P (2007) Measuring behavior: an introductory guide, 3rd edn. Cambridge University Press, Cambridge
Mcdonald JH (2014) Handbook of biological statistics, 3rd edn. Sparky House Publishing, Baltimore
Mendes N, Call J (2014) Chimpanzees form long-term memories for food locations after limited exposure. Am J Primatol 76:485–495. https://doi.org/10.1002/ajp.22248
Menzel EW, Juno C (1982) Marmosets (Saguinus fuscicollis): Are Learning Sets Learned? Science 217:750–752. https://doi.org/10.1126/science.217.4561.750
Miller CT (2017) Why marmosets? Dev Neurobiol 77:237–243. https://doi.org/10.1002/dneu.22483
Milton K (1981) Distribution patterns of tropical plant foods as an evolutionary stimulus to primate mental development. Am Anthropol 83:534–548
Nascimento SS, Alves JJA (2008) Ecoclimatologia do cariri paraibano. Rev Geográfica Acadêmica 2:28–41
Noser R, Byrne RW (2015) Wild chacma baboons (Papio ursinus) remember single foraging episodes. Anim Cogn 18:921–929. https://doi.org/10.1007/s10071-015-0862-4
Pesendorfer MB, Gunhold T, Schiel N, Souto A, Huber L, Range F (2009) The maintenance of traditions in marmosets: individual habit, not social conformity? A field experiment. PLoS ONE. https://doi.org/10.1371/journal.pone.0004472
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. https://doi.org/10.3758/BF03199010
Pontes ARM, Soares ML (2005) Sleeping sites of common marmosets (Callithrix jacchus) in defaunated urban forest fragments: a strategy to maximize food intake. J Zool 266:55–63. https://doi.org/10.1017/S095283690500662X
Poucet B (1993) Spatial cognitive maps in animals: new hypotheses on their structure and neural mechanisms. Psychol Rev 100:163–182. https://doi.org/10.1037/0033-295X.100.2.163
Powell LE, Isler K, Barton RA (2017) Re-evaluating the link between brain size and behavioural ecology in primates. Proc Biol Sci 284:20171765. https://doi.org/10.1098/rspb.2017.1765
Quirino ZGM (2006) Fenologia, síndromes de polinização e dispersão e recursos florais de uma comunidade de caatinga no cariri paraibano. Universidade Federal de Pernambuco, Tesis
R Core Team (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL https://www.R-project.org/
Raboy BE, Canale GR, Dietz JM (2008) Ecology of Callithrix kuhlii and a review of eastern Brazilian marmosets. Int J Primatol 29:449–467. https://doi.org/10.1007/s10764-008-9249-6
Raboy BE, Dietz JM (2004) Diet, foraging, and use of space in wild golden-headed lion tamarins. Am J Primatol 63:1–15. https://doi.org/10.1002/ajp.20032
Robert C, Casella G (2010) Introduction Monte Carlo methods with R. Springer, New York
Rylands AB, de Faria DS (1993) Habitats, feeding ecology, and home range size in the genus Callithrix. In: Rylands AB (ed) Marmosets and tamarins: systematics, behavior, and ecology. Oxford University Press, UK, pp 262–272
Schiel N, Souto A (2017) The common marmoset: an overview of its natural history, ecology and behavior. Dev Neurobiol 77:244–262. https://doi.org/10.1002/dneu.22458
Schiel N, Souto A, Huber L, Bezerra BM (2010) Hunting strategies in wild common marmosets are prey and age dependent. Am J Primatol 72:1039–1046. https://doi.org/10.1002/ajp.20860
Schwartz BL, Colon MR, Sanchez IC, Rodriguez I, Evans S (2002) Single-trial learning of "what" and "who" information in a gorilla (Gorilla gorilla gorilla): implications for episodic memory. Anim Cogn 5:85–90. https://doi.org/10.1007/s10071-002-0132-0
Schwartz BL, Evans S (2001) Episodic memory in primates. Am J Primatol 55:71–85. https://doi.org/10.1002/ajp.1041
Shettleworth SJ (2010) Cognition, evolution and behavior, 2nd edn. Oxford University Press, USA
Souto A, Bezerra BM, Schiel N, Huber L (2007) Saltatory search in free-living Callithrix jacchus: environmental and age influences. Int J Primatol 28:881–893. https://doi.org/10.1007/s10764-007-9165-1
Stevens JR, Hallinan EV, Hauser MD (2005) The ecology and evolution of patience in two New World monkeys. Biol Lett 1:223–226. https://doi.org/10.1098/rsbl.2004.0285
Stevens JR, Wood JN, Hauser MD (2007) When quantity trumps number: discrimination experiments in cotton-top tamarins (Saguinus oedipus) and common marmosets (Callithrix jacchus). Anim Cogn 10:429–437. https://doi.org/10.1007/s10071-007-0081-8
Teichroeb JA, Chapman CA (2014) Sensory information and associative cues used in food detection by wild vervet monkeys. Anim Cogn 17:517–528. https://doi.org/10.1007/s10071-013-0683-2
Trapanese C, Meunier H, Masi S (2018) What, where and when: spatial foraging decisions in primates. Biol Rev. https://doi.org/10.1111/brv.12462
Tsalyuk M, Kilian W, Reineking B, Getz WM (2019) Temporal variation in resource selection of African elephants follows long-term variability in resource availability. Ecol Monogr 89:1–19. https://doi.org/10.1002/ecm.1348
Tujague MP, Janson CH (2017) Foraging cognition in Neotropical primates: Integrating studies from the wild and from captivity. In: Kowalewski MM, Oklander LI (eds) Primatology in Argentina, III edn. Sociedad Argentina para Estudio de los Mamíferos SAREM, Buenos Aires, pp 151–170
Tujague MP, Janson CH, Lahitte HB (2015) Long-term spatial memory and learning set formation in captive capuchin monkeys (Cebus libidinosus = Sapajus cay). Int J Primatol 36:1067–1085. https://doi.org/10.1007/s10764-015-9878-5
Tulving E (2005) Episodic memory and autonoesis: uniquely human? In: Terrace HS, Metfalfe J (eds) The missing link in cognition: origins of self-reflective consciousness. Oxford University Press, Oxford, pp 3–56
Vannuchi CRS, Costa CS, de Jesus FM et al (2020) Sex, diurnal variation and retention interval differently affect performance of marmoset monkeys in a recognition memory task for object location. Behav Brain Res 379:112334. https://doi.org/10.1016/j.bbr.2019.112334
Acknowledgements
We thank Dr. Geraldo Baracuhy for providing the Baracuhy Biological Field Station to conduct our research. We are also grateful to María Fernanda De la Fuente, Júlia Vasconcelos, and Yara Lima for their support and help during data collection. We also would like to thank Dr. Paul Garber for his help and advice during an earlier draft of this manuscript. This study was funded by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) (PVE n°88881.064998/2014-01) and by a Ph.D. grant from Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) awarded to Filipa Abreu. The present study was conducted in accordance with Brazilian laws for the use of wild animals in research and was approved by Ethics Committee for Animal Use of the Federal Rural University of Pernambuco (license n°144/2014) and SISBio (license n°46770/1). In addition, the study has complied with the ethical standards in the treatment of their animals of University of Illinois for Animal Research (IACUC n°14263). The research adhered to the guidelines laid down by EC guide for animal experiments and Brazilian laws.
Funding
This study was funded by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) (PVE n°88881.064998/2014-01) and by a Ph.D. grant from Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) awarded to Filipa Abreu.
Author information
Authors and Affiliations
Contributions
All authors contributed to the study conception and design. Data collection and analysis were performed by FA. All authors wrote and reviewed the manuscript. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflicts of interest.
Ethical approval
All procedures performed involving animals were in accordance with Brazilian laws for the use of wild animals in research and were approved by Ethics Committee for Animal Use of the Federal Rural University of Pernambuco (license n° 144/2014) and SISBio (license n°46770/1). In addition, the study has complied with the ethical standards in the treatment of their animals of University of Illinois for Animal Research (IACUC n°14263).
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
About this article
Cite this article
Abreu, F., Souto, A. & Schiel, N. Wild common marmosets (Callithrix jacchus) employ spatial cognitive abilities to improve their food search and consumption: an experimental approach in small-scale space. Primates 61, 807–816 (2020). https://doi.org/10.1007/s10329-020-00826-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10329-020-00826-1