Social foragers can use either a ‘producer’ strategy, which involves searching for food, or a ‘scrounger’ strategy, which involves joining others' food discoveries. While producers rely on personal information and past experience, we may ask whether the tendency to forage as a producer is related to being a better learner. To answer this question, we hand-raised house sparrow (Passer domesticus) nestlings that upon independence were given an individual-learning task that required them to associate colour signal and food presence. Following the testing phase, all fledglings were released into a shared aviary, and their social-foraging tendencies were measured. We found a significant positive correlation between individual's performance in the individual-learning task and subsequent tendency to use searching (producing) behaviour. Individual-learning score was negatively correlated with initial fear of the test apparatus and with body weight. However, the correlation between individual learning and searching remained significant after controlling for these variables. Since it was measured before the birds entered a social group, individual-learning ability could not be the outcome of being a producer. However, the two traits may be initially associated, or individual learning could facilitate producing behaviour. To our knowledge, this is the first evidence that associates individual-learning abilities with social-foraging strategies in animal groups.

References

1
Slater P. J. B. . 1981 Individual differences in animal behavior. Perspectives in ethology (eds , Bateson P. P. G.& Klopfer P. H. ), pp. 35–49. New York, NY: Plenum. Crossref, Google Scholar
2
Clark A. B.& Ehlinger T. J. . 1987 Pattern and adaptation in individual behavioral differences. Perspectives in ethology (eds , Bateson P. P. G.& Klopfer P. H. ), pp. 1–47. New York, NY: Plenum Press. Crossref, Google Scholar
3
Stamps J. A. . 1991 Why evolutionary issues are reviving interest in proximate behavioral mechanisms. Am. Zool. 31, 338–348. Crossref, Google Scholar
4
Wilson D. S., Clark A. B., Coleman K.& Dearstyne T. . 1994 Shyness and boldness in humans and other animals. Trends Ecol. Evol. 9, 442–446. Crossref, ISI, Google Scholar
5
Wilson D. S. . 1998 Adaptive individual differences within single populations. Phil. Trans. R. Soc. Lond. B 353, 199–205.doi: 10.1098/rstb.1998.0202 (doi:10.1098/rstb.1998.0202). Link, ISI, Google Scholar
6
Sih A., Bell A. M., Johnson J. C.& Ziemba R. E. . 2004 Behavioral syndromes: an integrative overview. Q. Rev. Biol. 79, 241–277.doi: 10.1086/422893 (doi:10.1086/422893). Crossref, PubMed, ISI, Google Scholar
7
Groothuis T. G. G.& Carere C. . 2005 Avian personalities: characterization and epigenesis. Neurosci. Biobehav. Rev. 29, 137–150.doi: 10.1016/j.neubiorev.2004.06.010 (doi:10.1016/j.neubiorev.2004.06.010). Crossref, PubMed, ISI, Google Scholar
8
Reale D., Reader S. M., Sol D., McDougall P. T.& Dingemanse N. J. . 2007 Integrating animal temperament within ecology and evolution. Biol. Rev. 82, 291–318.doi: 10.1111/j.1469-185X.2007.00010.x (doi:10.1111/j.1469-185X.2007.00010.x). Crossref, PubMed, ISI, Google Scholar
9
Sih A.& Bell A. M. . 2008 Insights for behavioral ecology from behavioral syndromes. Advances in the study of behavior (eds , Brockman H. J., Roper T. J., Naguib M., Wynne-Edwards K. E., Barnard C.& Mitani J. C. ), vol. 38, pp. 227–281. San Diego, CA: Elsevier Academic Press Inc. Crossref, Google Scholar
10
Dall S. R. X., Houston A. I.& McNamara J. M. . 2004 The behavioural ecology of personality: consistent individual differences from an adaptive perspective. Ecol. Lett. 7, 734–739.doi: 10.1111/j.1461-0248.2004.00618.x (doi:10.1111/j.1461-0248.2004.00618.x). Crossref, ISI, Google Scholar
11
McElreath R.& Strimling P. . 2006 How noisy information and individual asymmetries can make ‘personality’ an adaptation: a simple model. Anim. Behav. 72, 1135–1139.doi: 10.1016/j.anbehav.2006.04.001 (doi:10.1016/j.anbehav.2006.04.001). Crossref, ISI, Google Scholar
12
Wolf M., van Doorn G. S., Leimar O.& Weissing F. J. . 2007 Life-history trade-offs favour the evolution of animal personalities. Nature 447, 581–584.doi: 10.1038/nature05835 (doi:10.1038/nature05835). Crossref, PubMed, ISI, Google Scholar
13
Wolf M., van Doorn G. S.& Weissing F. J. . 2008 Evolutionary emergence of responsive and unresponsive personalities. Proc. Natl Acad. Sci. USA 105, 15 825–15 830.doi: 10.1073/pnas.0805473105 (doi:10.1073/pnas.0805473105). Crossref, ISI, Google Scholar
14
Bateson P. . 1979 How do sensitive periods arise and what are they for. Anim. Behav. 27, 470–486.doi: 10.1016/0003-3472(79)90184-2 (doi:10.1016/0003-3472(79)90184-2). Crossref, ISI, Google Scholar
15
Nelson D. A.& Marler P. . 1993 Innate recognition of song in white-crowned sparrows—a role in selective vocal learning. Anim. Behav. 46, 806–808.doi: 10.1006/anbe.1993.1258 (doi:10.1006/anbe.1993.1258). Crossref, ISI, Google Scholar
16
Laland K. N.& Janik V. M. . 2006 The animal cultures debate. Trends Ecol. Evol. 21, 542–547.doi: 10.1016/j.tree.2006.06.005 (doi:10.1016/j.tree.2006.06.005). Crossref, PubMed, ISI, Google Scholar
17
Laland K. N. . 2004 Social learning strategies. Learn. Behav. 32, 4–14. Crossref, PubMed, ISI, Google Scholar
18
Boogert N. J., Reader S. M.& Laland K. N. . 2006 The relation between social rank, neophobia and individual learning in starlings. Anim. Behav. 72, 1229–1239.doi: 10.1016/j.anbehav.2006.02.021 (doi:10.1016/j.anbehav.2006.02.021). Crossref, ISI, Google Scholar
19
Boogert N. J., Reader S. M., Hoppitt W.& Laland K. N. . 2008 The origin and spread of innovations in starlings. Anim. Behav. 75, 1509–1518.doi: 10.1016/j.anbehav.2007.09.033 (doi:10.1016/j.anbehav.2007.09.033). Crossref, ISI, Google Scholar
20
Liker A.& Bokony V. . 2009 Larger groups are more successful in innovative problem solving in house sparrows. Proc. Natl Acad. Sci. USA 106, 7893–7898.doi: 10.1073/pnas.0900042106 (doi:10.1073/pnas.0900042106). Crossref, PubMed, ISI, Google Scholar
21
Mery F., Belay A. T., So A. K. C., Sokolowski M. B.& Kawecki T. J. . 2007 Natural polymorphism affecting learning and memory in Drosophila. Proc. Natl Acad. Sci. USA 104, 13 051–13 055.doi: 10.1073/pnas.0702923104 (doi:10.1073/pnas.0702923104). Crossref, ISI, Google Scholar
22
Matzel L. D., Townsend D. A., Grossman H., Han Y. R., Hale G., Zappulla M., Light K.& Kolata S. . 2006 Exploration in outbred mice covaries with general learning abilities irrespective of stress reactivity, emotionality, and physical attributes. Neurobiol. Learn. Mem. 86, 228–240.doi: 10.1016/j.nlm.2006.03.004 (doi:10.1016/j.nlm.2006.03.004). Crossref, PubMed, ISI, Google Scholar
23
Matzel L. D., Han Y. R., Grossman H., Karnik M. S., Patel D., Scott N., Specht S. M.& Gandhi C. C. . 2003 Individual differences in the expression of a ‘general’ learning ability in mice. J. Neurosci. 23, 6423–6433. Crossref, PubMed, ISI, Google Scholar
24
Barnard C. J.& Sibly R. M. . 1981 Producers and scroungers—a general-model and its application to captive flocks of house sparrows. Anim. Behav. 29, 543–550.doi: 10.1016/S0003-3472(81)80117-0 (doi:10.1016/S0003-3472(81)80117-0). Crossref, ISI, Google Scholar
25
Bell A. M. . 2007 Future directions in behavioural syndromes research. Proc. R. Soc. B 274, 755–761.doi: 10.1098/rspb.2006.0199 (doi:10.1098/rspb.2006.0199). Link, ISI, Google Scholar
26
Giraldeau L. A.& Caraco T. . 2000 Social foraging theory. Princeton, NJ: Princeton University Press. Crossref, Google Scholar
27
Giraldeau L. A.& Dubois F. . 2008 Social foraging and the study of exploitative behavior. Advances in the study of behavior (eds , Brockman H. J., Roper T. J., Naguib M., Wynne-Edwards K. E., Barnard C.& Mitani J. C. ), vol. 38, pp. 59–104. San Diego, CA: Elsevier Academic Press Inc. Google Scholar
28
Kurvers R. H. J. M., Prins H. H. T., van Wieren S. E., van Oers K., Nolet B. A.& Ydenberg R. C. . 2010 The effect of personality on social foraging: shy barnacle geese scrounge more. Proc. R. Soc. B 277, 601–608.doi: 10.1098/rspb.2009.1474 (doi:10.1098/rspb.2009.1474). Link, ISI, Google Scholar
29
Beauchamp G. . 2006 Phenotypic correlates of scrounging behavior in zebra finches: role of foraging efficiency and dominance. Ethology 112, 873–878.doi: 10.1111/j.1439-0310.2006.01241.x (doi:10.1111/j.1439-0310.2006.01241.x). Crossref, ISI, Google Scholar
30
Liker A.& Barta Z. . 2002 The effects of dominance on social foraging tactic use in house sparrows. Behaviour 139, 1061–1076.doi: 10.1163/15685390260337903 (doi:10.1163/15685390260337903). Crossref, ISI, Google Scholar
31
Marchetti C.& Drent P. J. . 2000 Individual differences in the use of social information in foraging by captive great tits. Anim. Behav. 60, 131–140.doi: 10.1006/anbe.2000.1443 (doi:10.1006/anbe.2000.1443). Crossref, PubMed, ISI, Google Scholar
32
Giraldeau L. A.& Lefebvre L. . 1986 Exchangeable producer and scrounger roles in a captive flock of feral pigeons—a case for the skill pool effect. Anim. Behav. 34, 797–803.doi: 10.1016/S0003-3472(86)80064-1 (doi:10.1016/S0003-3472(86)80064-1). Crossref, ISI, Google Scholar
33
Beauchamp G. . 2001 Consistency and flexibility in the scrounging behaviour of zebra finches. Can. J. Zool. 79, 540–544.doi: 10.1139/cjz-79-3-540 (doi:10.1139/cjz-79-3-540). Crossref, ISI, Google Scholar
34
Morand-Ferron J., Giraldeau L. A.& Lefebvre L. . 2007 Wild carib grackles play a producer–scrounger game. Behav. Ecol. 18, 916–921.doi: 10.1093/beheco/arm058 (doi:10.1093/beheco/arm058). Crossref, ISI, Google Scholar
35
Morand-Ferron J.& Giraldeau L. A. . 2010 Learning behaviorally stable solutions to producer–scrounger games. Behav. Ecol. 21, 343–348.doi: 10.1093/beheco/arp195 (doi:10.1093/beheco/arp195). Crossref, ISI, Google Scholar
36
Giraldeau L. A., Valone T. J.& Templeton J. J. . 2002 Potential disadvantages of using socially acquired information. Phil. Trans. R. Soc. Lond. B 357, 1559–1566.doi: 10.1098/rstb.2002.1065 (doi:10.1098/rstb.2002.1065). Link, ISI, Google Scholar
37
Kameda T.& Nakanishi D. . 2002 Cost-benefit analysis of social/cultural learning in a nonstationary uncertain environment—an evolutionary simulation and an experiment with human subjects. Evol. Hum. Behav. 23, 373–393.doi: 10.1016/S1090-5138(02)00101-0 (doi:10.1016/S1090-5138(02)00101-0). Crossref, ISI, Google Scholar
38
Dall S. R. X., Giraldeau L. A., Olsson O., McNamara J. M.& Stephens D. W. . 2005 Information and its use by animals in evolutionary ecology. Trends Ecol. Evol. 20, 187–193.doi: 10.1016/j.tree.2005.01.010 (doi:10.1016/j.tree.2005.01.010). Crossref, PubMed, ISI, Google Scholar
39
Bicca-Marques J. C.& Garber P. A. . 2005 Use of social and ecological information in tamarin foraging decisions. Int. J. Primatol. 26, 1321–1344.doi: 10.1007/s10764-005-8855-9 (doi:10.1007/s10764-005-8855-9). Crossref, ISI, Google Scholar
40
Katsnelson E., Motro U., Feldman M. W.& Lotem A. . 2008 Early experience affects producer–scrounger foraging tendencies in the house sparrow. Anim. Behav. 75, 1465–1472.doi: 10.1016/j.anbehav.2007.09.020 (doi:10.1016/j.anbehav.2007.09.020). Crossref, ISI, Google Scholar
41
Belmaker A. . 2007 Learning to choose between foraging strategies in adult house sparrows. MS thesis, Tel-Aviv University, Tel Aviv, Israel. [in Hebrew.]. Google Scholar
42
Gionfriddo J. P.& Best L. B. . 1996 Grit color selection by house sparrows and northern bobwhites. J. Wildl. Manage. 60, 836–842. Crossref, ISI, Google Scholar
43
Coolen I. . 2002 Increasing foraging group size increases scrounger use and reduces searching efficiency in nutmeg mannikins (Lonchura punctulata). Behav. Ecol. Sociobiol. 52, 232–238.doi: 10.1007/s00265-002-0500-4 (doi:10.1007/s00265-002-0500-4). Crossref, ISI, Google Scholar
44
Sokal R. R.& Rohlf F. J. . 1981 Biometry, 2nd edn. San Francisco, CA: Freeman and Company. Google Scholar
45
Sheskin D. J. . 2004 Handbook of parametric and nonparametric statistical procedures, 3rd edn, p. 1071. Boca Raton, FL: CRC Press. Google Scholar
46
Seferta A., Guay P. J., Marzinotto E.& Lefebvre L. . 2001 Learning differences between feral pigeons and zenaida doves: the role of neophobia and human proximity. Ethology 107, 281–293.doi: 10.1046/j.1439-0310.2001.00658.x (doi:10.1046/j.1439-0310.2001.00658.x). Crossref, ISI, Google Scholar
47
Webster S. J.& Lefebvre L. . 2001 Problem solving and neophobia in a columbiform–passeriform assemblage in Barbados. Anim. Behav. 62, 23–32.doi: 10.1006/anbe.2000.1725 (doi:10.1006/anbe.2000.1725). Crossref, ISI, Google Scholar
48
Greenberg R. . 2003 The role of neophobia and neophilia in the development of innovative behaviour of birds. Animal innovation (eds , Reader S. M.& Laland K. N. ), pp. 175–196. New York, NY: Oxford University Press. Crossref, Google Scholar
49
Cassady J. C.& Johnson R. E. . 2002 Cognitive test anxiety and academic performance. Contemp. Educ. Psychol. 27, 270–295.doi: 10.1006/ceps.2001.1094 (doi:10.1006/ceps.2001.1094). Crossref, ISI, Google Scholar
50
Spencer K. A., Buchanan K. A., Goldsmith A. R.& Catchpole C. K. . 2003 Song as an honest signal of developmental stress in the zebra finch (Taeniopygia guttata). Horm. Behav. 79, 241–277. Google Scholar
51
Johnson E. O.& Breslau N. . 2000 Increased risk of learning disabilities in low birth weight boys at age 11 years. Biol. Psychiatry 47, 490–500.doi: 10.1016/S0006-3223(99)00223-1 (doi:10.1016/S0006-3223(99)00223-1). Crossref, PubMed, ISI, Google Scholar
52
Hack M., Flannery D. J., Schluchter M., Cartar L., Borawski E.& Klein N. . 2002 Outcomes in young adulthood for very-low-birth-weight infants. N. Engl. J. Med. 346, 149–157.doi: 10.1056/NEJMoa010856 (doi:10.1056/NEJMoa010856). Crossref, PubMed, ISI, Google Scholar
53
Lofdahl K. L., Holliday M.& Hirsch J. . 1992 Selection for conditionability in Drosophila melanogaster. J. Comp. Psychol. 106, 172–183.doi: 10.1037/0735-7036.106.2.172 (doi:10.1037/0735-7036.106.2.172). Crossref, PubMed, ISI, Google Scholar
54
Mery F.& Kawecki T. J. . 2002 Experimental evolution of learning ability in fruit flies. Proc. Natl Acad. Sci. USA 99, 14 274–14 279.doi: 10.1073/pnas.222371199 (doi:10.1073/pnas.222371199). Crossref, ISI, Google Scholar
55
Dukas R. . 2004 Evolutionary biology of animal cognition. Ann. Rev. Ecol. Evol. Syst. 35, 347–374.doi: 10.1146/annurev.ecolsys.35.112202.130152 (doi:10.1146/annurev.ecolsys.35.112202.130152). Crossref, ISI, Google Scholar
56
Galsworthy M. J., Paya-Cano J. L., Liu L., Monleon S., Gregoryan G., Fernandes C., Schalkwyk L. C.& Plomin R. . 2005 Assessing reliability, heritability and general cognitive ability in a battery of cognitive tasks for laboratory mice. Behav. Genet. 35, 675–692.doi: 10.1007/s10519-005-3423-9 (doi:10.1007/s10519-005-3423-9). Crossref, PubMed, ISI, Google Scholar
57
Arbilly M., Motro U., Feldman M. W.& Lotem A. Submitted. Co-evolution of learning and social strategies: I. complex and simple learning rules in the producer–scrounger game. Google Scholar
58
Laland K. N., Odling-Smee J.& Gilbert S. F. . 2008 EvoDevo and niche construction: building bridges. J. Exp. Zool. B Mol. Dev. Evol. 310B, 549–566.doi: 10.1002/jez.b.21232 (doi:10.1002/jez.b.21232). Crossref, ISI, Google Scholar