Differential patch-leaving behavior during probabilistic foraging in humans and gerbils.
Journal
Communications biology
ISSN: 2399-3642
Titre abrégé: Commun Biol
Pays: England
ID NLM: 101719179
Informations de publication
Date de publication:
15 Aug 2024
15 Aug 2024
Historique:
received:
19
01
2023
accepted:
06
08
2024
medline:
16
8
2024
pubmed:
16
8
2024
entrez:
15
8
2024
Statut:
epublish
Résumé
Foraging confronts animals, including humans, with the need to balance exploration and exploitation: exploiting a resource until it depletes and then deciding when to move to a new location for more resources. Research across various species has identified rules for when to leave a depleting patch, influenced by environmental factors like patch quality. Here we compare human and gerbil patch-leaving behavior through two analogous tasks: a visual search for humans and a physical foraging task for gerbils, both involving patches with randomly varying initial rewards that decreased exponentially. Patch-leaving decisions of humans but not gerbils follow an incremental mechanism based on reward encounters that is considered optimal for maximizing reward yields in variable foraging environments. The two species also differ in their giving-up times, and some human subjects tend to overharvest. However, gerbils and individual humans who do not overharvest are equally sensitive to declining collection rates in accordance with the marginal value theorem. Altogether this study introduces a paradigm for a between-species comparison on how to resolve the exploitation-exploration dilemma.
Identifiants
pubmed: 39147833
doi: 10.1038/s42003-024-06683-8
pii: 10.1038/s42003-024-06683-8
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
1000Subventions
Organisme : Deutsche Forschungsgemeinschaft (German Research Foundation)
ID : 425899996e CRC 1436 (sub-project C02)
Informations de copyright
© 2024. The Author(s).
Références
Pyke, G. H. Optimal foraging theory: a critical review. Annu. Rev. Ecol. Syst. 15, 523–575 (1984).
doi: 10.1146/annurev.es.15.110184.002515
Sih, A. Understanding variation in behavioural responses to human-induced rapid environmental change: a conceptual overview. Anim. Behav. 85, 1077–1088 (2013).
doi: 10.1016/j.anbehav.2013.02.017
Kristjánsson, Á., Björnsson, A. S. & Kristjánsson, T. Foraging with Anne Treisman: Features versus conjunctions, patch leaving and memory for foraged locations. Atten. Percept. Psychophys. 82, 818–831 (2020).
doi: 10.3758/s13414-019-01941-y
pubmed: 31898061
Wolfe, J. M. When is it time to move to the next raspberry bush? Foraging rules in human visual search. J. Vis. 13, 1–17 (2013).
doi: 10.1167/13.3.10
Daw, N. D., O’doherty, J. P., Dayan, P., Seymour, B. & Dolan, R. J. Cortical substrates for exploratory decisions in humans. Nature 441, 876–879 (2006).
doi: 10.1038/nature04766
pubmed: 16778890
pmcid: 2635947
Laureiro‐Martínez, D., Brusoni, S., Canessa, N. & Zollo, M. Understanding the exploration–exploitation dilemma: an fMRI study of attention control and decision‐making performance. Strateg. Manag. J. 36, 319–338 (2015).
doi: 10.1002/smj.2221
Lottem, E. et al. Activation of serotonin neurons promotes active persistence in a probabilistic foraging task. Nat. Commun. 9, 1–12 (2018).
doi: 10.1038/s41467-018-03438-y
Charnov, E. L. Optimal foraging, the marginal value theorem. Theor. Popul. Biol. 9, 129–136 (1976).
doi: 10.1016/0040-5809(76)90040-X
pubmed: 1273796
Green, R. F. Stopping rules for optimal foragers. Am. Nat. 123, 30–43 (1984).
doi: 10.1086/284184
Krebs, J. R., Ryan, J. C. & Charnov, E. L. Hunting by expectation or optimal foraging? A study of patch use by chickadees. Anim. Behav. 22, 953–964 (1974).
doi: 10.1016/0003-3472(74)90018-9
Wajnberg, E., Bernhard, P., Hamelin, F. & Boivin, G. Optimal patch time allocation for time-limited foragers. Behav. Ecol. Sociobiol. 60, 1–10 (2006).
doi: 10.1007/s00265-005-0131-7
Wilke, A., Hutchinson, J. M., Todd, P. M. & Czienskowski, U. Fishing for the right words: decision rules for human foraging behavior in internal search tasks. Cogn. Sci. 33, 497–529 (2009).
doi: 10.1111/j.1551-6709.2009.01020.x
pubmed: 21585478
Iwasa, Y., Higashi, M. & Yamamura, N. Prey distribution as a factor determining the choice of optimal foraging strategy. Am. Nat. 117, 710–723 (1981).
doi: 10.1086/283754
Waage, J. K. Foraging for patchily-distributed hosts by the parasitoid, Nemeritis canescens. J. Anim. Ecol. https://doi.org/10.2307/4166 (1979).
McNair, J. N. Optimal giving-up times and the marginal value theorem. Am. Nat. 119, 511–529 (1982).
doi: 10.1086/283929
Hutchinson, J. M., Wilke, A. & Todd, P. M. Patch leaving in humans: can a generalist adapt its rules to dispersal of items across patches? Anim. Behav. 75, 1331–1349 (2008).
doi: 10.1016/j.anbehav.2007.09.006
Mata, R., Wilke, A. & Czienskowski, U. Cognitive aging and adaptive foraging behavior. J. Gerontol. Ser. B 64, 474–481 (2009).
doi: 10.1093/geronb/gbp035
Bender, R. Introduction to the use of regression models in epidemiology. Cancer Epidemiol. https://doi.org/10.1007/978-1-59745-416-2_9 (2009).
Stephens, D. W. & Krebs, J. R. Foraging Theory. (Princeton University Press, Princeton, 1987).
Redhead, E. & Tyler, P. A. An experimental analysis of optimal foraging behaviour in patchy environments. Q. J. Exp. Psychol. Sect. B 40, 83–102 (1988).
Ydenberg, R. C. Great tits and giving-up times: decision rules for leaving patches. Behaviour 90, 1–24 (1984).
doi: 10.1163/156853984X00533
Mata, R., Wilke, A. & Czienskowski, U. Foraging across the life span: is there a reduction in exploration with aging? Front. Neurosci. 7, 53 (2013).
doi: 10.3389/fnins.2013.00053
pubmed: 23616741
pmcid: 3627975
Raio, C. et al. Heterogeneity in foraging decisions relates to drug addiction and is a marker of midbrain dopamine function. Biol. Psychiatry 89, S239 (2021).
doi: 10.1016/j.biopsych.2021.02.599
Grether, G. F., Palombit, R. A. & Rodman, P. S. Gibbon foraging decisions and the marginal value model. Int. J. Primatol. 13, 1–17 (1992).
doi: 10.1007/BF02547724
Barack, D. L. et al. Attention deficits linked with proclivity to explore while foraging. Proc. R. Soc. B 291, 20222584 (2024).
doi: 10.1098/rspb.2022.2584
pubmed: 38378153
Mansouri, F. A., Koechlin, E., Rosa, M. G. & Buckley, M. J. Managing competing goals—a key role for the frontopolar cortex. Nat. Rev. Neurosci. 18, 645–657 (2017).
doi: 10.1038/nrn.2017.111
pubmed: 28951610
Güldener, L., & Pollmann, S. Behavioral bias for exploration is associated with enhanced signaling in the lateral and medial frontopolar cortex. J. Cogn. Neurosci. https://doi.org/10.1162/jocn_a_02132 (2024).
Pollmann, S. Frontopolar resource allocation in human and nonhuman primates. Trends Cogn. Sci. 20, 84–86 (2016).
doi: 10.1016/j.tics.2015.11.006
pubmed: 26699223
Zajkowski, W. K., Kossut, M. & Wilson, R. C. A causal role for right frontopolar cortex in directed, but not random, exploration. Elife 6, e27430 (2017).
doi: 10.7554/eLife.27430
pubmed: 28914605
pmcid: 5628017
Mansouri, F. A., Buckley, M. J., Mahboubi, M. & Tanaka, K. Behavioral consequences of selective damage to frontal pole and posterior cingulate cortices. Proc. Natl Acad. Sci. USA 112, E3940–E3949 (2015).
doi: 10.1073/pnas.1422629112
pubmed: 26150522
pmcid: 4517212
Pollmann, S. et al. Selective visual dimension weighting deficit after left lateral frontopolar lesions. J. Cogn. Neurosci. 19, 365–375 (2007).
doi: 10.1162/jocn.2007.19.3.365
pubmed: 17335386
Laubach, M., Amarante, L. M., Swanson, K., & White, S. R. What, if anything, is rodent prefrontal cortex? Eneuro https://doi.org/10.1523/ENEURO.0315-18.2018 (2018).
Birke, L. I., D’Udine, B. & Albonetti, M. E. Exploratory behavior of two species of murid rodents, Acomys cahirinus and Mus musculus: a comparative study. Behav. Neural Biol. 43, 143–161 (1985).
doi: 10.1016/S0163-1047(85)91337-8
pubmed: 4004686
Peirce, J. et al. PsychoPy2: experiments in behavior made easy. Behav. Res. Methods 51, 195–203 (2019).
doi: 10.3758/s13428-018-01193-y
pubmed: 30734206
pmcid: 6420413
Cain, M. S., Vul, E., Clark, K. & Mitroff, S. R. A Bayesian optimal foraging model of human visual search. Psychol. Sci. 23, 1047–1054 (2012).
doi: 10.1177/0956797612440460
pubmed: 22868494
Vallat, R. Pingouin: statistics in Python. J. Open Source Softw. 3, 1026 (2018).
doi: 10.21105/joss.01026
Güldener, L. et al. Behavioral data of humans and animsl. OSF Repository https://doi.org/10.17605/OSF.IO/FEXGB (2023).