The history of scatter hoarding studies

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 365, Issue 1542, 2010, Pages 869-881

  Brodin, Anders ^a  

^a LUND UNIVERSITY   (Sweden)

Author keywords

Cache retrieval; Hippocampus; Optimal cache density; Scatter hoarding; Spatial memory

Indexed keywords

BRAIN; CACHING; COEVOLUTION; EVOLUTIONARY BIOLOGY; GAME THEORY; MEMORY; OPTIMIZATION; ORNITHOLOGY; THEORETICAL STUDY;

ANIMALIA; AVES; NUCIFRAGA; PARIDAE; SCIURIDAE;

EID: 77950261495     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2009.0217     Document Type: Review

References (112)

1. Andersson, M. & Krebs, J. 1978 On the evolution of hoarding behaviour. Anim. Behav. 26, 707-711. (doi:10.1016/ 0003-3472(78)90137-9)
2. Baker, M. C., Stone, E., Miller Baker, A. E., Shelden, R. J., Skillicorn, P. & Mantych, M. D. 1988 Evidence against observational learning in storage and recovery of seeds by black-capped chickadees. Auk 105, 492-497.
3. Balda, R. P. & Kamil, A. C. 1992 Long-term spatial memory in Clark's nutcracker, Nucifraga columbiana. Anim. Behav. 44, 761-769. (doi:10.1016/S0003- 3472(05)80302-1)
4. Balda, R. P. & Kamil, A. C. 2006 Linking life zones, life history traits, ecology, and spatial cognition in four allopatric southwestern seed caching corvids. In Animal spatial cognition, online cyberbook (eds M. Brown & R. Cook), pp. 761-769. Comparative Cognition Society.
5. Barnea, A. & Nottebohm, F. 1994 Seasonal recruitment of hippocampal neurons in adult free-ranging black-capped chickadees. Proc. Natl Acad. Sci. USA 91, 11217-11 221. (doi:10.1073/pnas.91.23.11217)
6. Bednekoff, P. A. & Balda, R. P. 1996 Social caching and observational spatial memory in pinyon jays. Behaviour 133, 807-826. (doi: 10.1163/156853996X00251)
7. Bolhuis, J. J. & Macphail, E. M. 2001 A critique of the neuroecology of learning and memory. Trends Cogn. Sci. (Regul. Ed.) 5, 426-433. (doi:10.1016/S1364-6613(00) 01753-8)
8. Bolhuis, J. J. & Macphail, E. M. 2002 Everything in neuroecology makes sense in the light of evolution. Trends Cogn. Sci. (Regul. Ed.) 6, 7-8. (doi:10.1016/S1364-6613(00) 01829-5)
9. Bossema, I. 1979 Jays and oaks: an eco-ethological study of symbiosis. Behaviour 70, 1-116. (doi: 10.1163/ 156853979X00016)
10. Brodbeck, D. R. 1994 Memory of spatial and local cues: a comparison of a storing and a nonstoring species. Anim. Learn. Behav. 22, 119-133.
11. Brodin, A. 1992 Cache dispersion affects retrieval time in hoarding willow tits. Ornis Scand. 23, 7-12. (doi: 10. 2307/3676420)
12. Brodin, A. 1993a Low rate of loss of willow tit caches may increase the adaptiveness of long-term hoarding. Auk 110, 642-645.
13. Brodin, A. 1993b Radio-ptilochronology-tracing radioactively labelled food in feathers. Omis Scand. 24, 167-173. (doi: 10.2307/3676732)
14. Brodin, A. 1994a The disappearance of caches that have been stored by naturally foraging willow tits Parus montanus. Anim. Behav. 47, 730-732. (doi:10.1006/ anbe.1994.1100)
15. Brodin, A. 1994b Separation of caches between individual willow tits hoarding under natural conditions. Anim. Behav. 47, 1031-1035. (doi:10.1006/anbe.1994.1141)
16. Brodin, A. 1994c The role of naturally stored food supplies in the winter diet of the boreal willow tit Parus montanus. Ornis Svecica 4, 31-40.
17. Brodin, A. 2005a Hippocampus volume does not correlate to food hoarding rates in the field in two closely related bird species, the black-capped chickadee Poecile atricapilla and the willow tit Parus montanus. Auk 122, 819-828. (doi:10.1642/0004-8038(2005)122[0819:HVDNCW]2.0. CO;2)
18. Brodin, A. 2005b Mechanisms of cache retrieval in longterm hoarding birds. J. Ethol. 23, 77-83. (doi:10.1007/ S10164-005-0147-155)
19. Brodin, A. & Bolhuis, J. J. 2008 Memory and brain in foodstoring birds: space oddities or adaptive specializations? Ethology 114, 1-13.
20. Brodin, A. & Ekman, J. 1994 Benefits of food hoarding. Nature372, 510. (doi:10.1038/372510a0)
21. Brodin, A. & Kunz, C. 1997 An experimental study of cache recovery by hoarding willow tits after different retention intervals. Behaviour 134, 881-890. (doi:10.1163/ 156853997X00205)
22. Brodin, A. & Lundborg, K. 2003 Is hippocampal volume affected by specialization for food hoarding in birds? Proc. R. Soc. Lond. B 270, 1555-1563. (doi:10.1098/ rspb.2003.2413)
23. Brodin, A., Lundborg, K. & Clark, C. W. 2001 The effect of dominance on food hoarding: a game theoretical model. Am. Nat. 157, 66-75. (doi:10.1086/317008)
24. Clarke, M. F. & Kramer, D. L. 1994 Scatter-hoarding by a larder-hoarding rodent: intraspecific variation in the hoarding behaviour of the Eastern chipmunk, Tamias striatus. Anim. Behav. 48, 299-308. (doi:10.1006/anbe. 1994.1243)
25. Clarkson, K., Eden, S. F., Sutherland, W. J. & Houston, A. I. 1986 Density dependence and magpie food hoarding. J. Anim. Ecol. 55, 111-121.
26. Clayton, N. S. & Dickinson, A. 1999 Memory for the content of caches by scrub jays (Aphelocoma coerulescens). J. Exp. Psychol. Anim. Behav. Process. 25, 82-91. (doi: 10.1037/0097-7403.25.1.82)
27. Clayton, S. S. & Krebs, J. R. 1994 Memory for spatial and object-specific cues in food-storing and non-storing birds. J. Comp. Physiol. B 174, 371-379.
28. Corkin, S. 2002 What's new with the amnesiac patient H.M.? Nature Rev. Neurosci. 3, 153-160. (doi:10.1038/nrn726)
29. Cowie, R. J., Krebs, J. R. & Sherry, D. F. 1981 Food storing by marsh tits. Anim. Behav. 29, 1252-1259. (doi:10. 1016/S0003-3472(81)80077-2)
30. Cristol, D. A. 1996 Food-storing does not affect hippocampal volume in experienced adult willow tits. Behav. Brain Res. 81, 233-236. (doi:10.1016/S0166-4328(96) 89083-8)
31. Darley-Hill, S. & Johnson, W. C. 1981 Acorn dispersal by the blue jay (Cyanocitta cristata). Oecologia 50, 231-232. (doi:10.1007/BF00348043)
32. Dwyer, D. M. & Clayton, N. S. 2002 A reply to the defenders of the faith. Trends Cogn. Sci. (Regul. Ed.) 6, 109-111. (doi:10.1016/S1364-6613(00) 01857-X)
33. Ekman, J. 1989 Ecology of non-breeding social systems of Parus. Wilson Bull. 101, 263-288.
34. Ekman, J., Brodin, A. & Sklepkovych, B. 1995 Selfish longterm benefits of hoarding in the Siberian jay. Behav. Ecol. 7, 140-144. (doi:10.1093/beheco/7.2.140)
35. Emery, N. J., Dally, J. M. & Clayton, N. S. 2003 Western scrub-jays (Aphelocoma californica) use cognitive strategies to protect their caches from thieving conspecifics. Anim. Cogn. 7, 37-43. (doi:10.1007/s10071-003-0178-7)
36. Francis, R. C. 2005 It's a puzzle all right: the hippocampus and food hoarding. Trends Ecol. Evol. 20, 476-477. (doi:10.1016/j.tree.2005.07.002)
37. Gibb, J. A. 1960 Populations of tits and goldcrests and their food supply in pine plantations. Ibis 102, 162-208.
38. Griffiths, D., Dickinson, A. & Clayton, N. 1999 Episodic memory: what can animals remember about their past? Trends Cogn. Sci. 3, 74-79. (doi:10.1016/S1364-6613(98)01272-8)
39. Grubb Jr, T. C. 1989 Ptilochronology: feather growth bars as indicators of nutritional status. Auk 106, 314-320.
40. Haftorn, S. 1956a Contributions to the food biology of tits especially about storing of surplus food. Part 3, the willow tit (Parus atricapillus L.). Kgl Nor. Vidensk. Selsk. Skr. 3, 1-80.
41. Haftorn, S. 1956e Contributions to the food biology of tits especially about storing of surplus food. Part 4, a comparative analysis of Parus atricapillus L., P cristatus L. and P. ater L. Kgl Nor. Vidensk. Selsk. Skr. 4, 1-54.
42. Haftorn, S. 1959 The proportion of spruce seeds removed by the tits in a Norwegian spruce forest in 1954-55. Kgl. Nor. Vidensk. Selsk. Forh. 32, 121-125.
43. Hampton, R. R. & Shettleworth, S. J. 1996 Hippocampal lesions impair memory for location but not color in passerine birds. Behav. Neurosci. 110, 831-835. (doi:10. 1037/0735-7044.110.4.831)
44. Hampton, R. R., Sherry, D. F., Shettleworth, S. J., Khurgel, M. & Ivy, G. 1995 Hippocampal volume and food-storing behavior are related in parids. Brain Behav. Evol. 45, 54-61. (doi:10.1159/000113385)
45. Hampton, R. R., Healy, S. D., Shettleworth, S. J. & Kamil, A. C. 2002 Neuroecologists are not made of straw. Trends Cogn. Sci. (Regul. Ed.) 6, 6-7. (doi:10.1016/S1364-6613(00)01821-0)
46. Healy, S. D. & Krebs, J. R. 1992 Food storing and the hippocampus in corvids: amount and volume are correlated. Proc. R. Soc. Lond. B 248, 241-245. (doi:10.1098/rspb. 1992.0068)
47. Healy, S. D. & Krebs, J. R. 1996 Food storing and the hippocampus in Paridae. Brain Behav. Evol. 47, 195-199. (doi:10.1159/000113239)
48. Healy, S. D. & Rowe, C. 2007 A critique of comparative studies of brain size. Proc. R. Soc. B 274, 453-464. (doi:10.1098/rspb.2006.3748)
49. Healy, S. D., Clayton, N. S. & Krebs, J. R. 1994 Development of hippocampal specialization in two species of tits. Behav. Brain Res. 61, 23-28. (doi:10.1016/0166-4328(94)90004-3)
50. Healy, S. D., de Kort, S. R. & Clayton, N. S. 2005 The hippocampus, spatial memory and food hoarding: a puzzle revisited. Trends Ecol. Evol. 20, 17-22. (doi:10.1016/j. tree.2004.10.006)
51. Hitchcock, C. L. & Sherry, D. F. 1990 Long-term memory for cache sites in the black-capped chickadee. Anim. Behav. 40, 701-712. (doi:10.1016/S0003-3472(05)80699-2)
52. Hoshooley, J. S., Phillmore, L. S., Sherry, D. F. & Macdougall-Shackleton, S. A. 2006 Annual cycle of the black-capped chickadee: seasonality of food-storing and the hippocampus. Brain Behav. Evol. 69, 161-168. (doi: 10.1159/000096984)
53. Hurly, T. A. & Robertson, R. J. 1987 Scatterhoarding by territorial red squirrels: a test of the optimal density model. Can. J. Zool. 65, 1247-1252. (doi:10.1139/z87-194)
54. Jacobs, L. F. & Liman, E. R. 1991 Grey squirrels remember the locations of buried nuts. Anim. Behav. 41, 103-110. (doi:10.1016/S0003-3472(05) 80506-8)
55. James, P. C. & Verbeek, N. A. M. 1984 Temporal and energetic aspects of food storage in northwestern crows. Ardea 72, 207-215.
56. Jansson, C. 1982 The year round diets of the willow tit Parus montanus Conrad and the crested tit P cristatus L. PhD thesis, Göteborgs Universitet, Göteborg.
57. Jerison, H. J. 1973 Evolution of the brain and intelligence. New York, NY: Academic Press.
58. Kraus, B. 1983 A test of the optimal-density model for seed scatterhoarding. Ecology 64, 608-610. (doi:10.2307/ 1939982)
59. Krebs, J. R., Sherry, D. F., Healy, S. D., Perry, V. H. & Vaccarino, A. L. 1989 Hippocampal specialization of food-storing birds. Proc. Natl Acad. Sci. USA 89, 1388-1392.
60. Krebs, J. R., Healy, S. D. & Shettleworth, S. J. 1990 Spatial memory of Paridae: comparison of a storing and a nonstoring species, the coal tit, Parus ater, and the great tit P. major. Anim. Behav. 39, 1127-1137. (doi:10.1016/ S0003-3472(05)80785-7)
61. Krebs, J. R., Clayton, N. S., Hampton, R. R. & Shettleworth, S. J. 1995 Effects of photoperiod on foodstoring and the hippocampus in a food-storing and a non-storing passerine bird. Neuroreport 16, 1701-1704.
62. Krushinskaya, N. L. 1966 Some complex forms of feeding behaviour of nutcracker Nucifraga caryocatactes, after removal of old cortex. Zh. Evol. Biokhim. Fiziol. 11, 563-568.
63. Lens, L., Adriaensen, F. & Dhondt, A. A. 1994 Age-related hoarding strategies in the crested tit Parus cristatus: should the cost of subordination be reassessed? J. Anim. Ecol. 63, 1-7.
64. Löhrl, H. 1950 Beobachtungen zur sociologie und Verhaltensweise von sumpfmeiser (Parus palustris communis) im winter. Z. Tierpsychol. 7, 417-424.
65. Löhrl, H. 1956 Das verhalten des kleibers (Sitta europaea caesia Wolf). Staatlichen vogelschutzwarte für BadenWärtemberg. Ludwigsburg 0, 191-252.
66. Lönnberg, E. 1913 Sp. 6 Caryocatactes. In Linnés föreläsningar over djurriket (Linnaeus lectures over the animal kingdom). Uppsala: Akademiska Bokhandeln.
67. Lucas, J. R., Brodin, A., de Kort, S. R. & Clayton, N. S. 2004 Does hippocampal volume size correlate with the degree of caching specialization? Proc. R. Soc. Lond. B 271, 2423-2429. (doi:10.1098/rspb.2004.2912)
68. Macdougall-Shackleton, S. A., Sherry, D. F., Clark, A. P., Pinkus, R. & Hernandez, A. M. 2003 Photoperiodic regulation of food-storing and hippocampus volume in black-capped chickadees, Poecile atricapilla. Anim. Behav. 64, 765-770.
69. Maynard Smith, J. 1982 Evolution and the theory of games. Cambridge, UK: Cambridge University Press.
70. Moreno, J., Lundberg, A. & Carlson, A. 1981 Hoarding of individual nuthatches Sitta europaea and marsh tits Parus palustris. Holarct. Ecol. 4, 263-269.
71. Morris, D. 1962 The behaviour of the green agouchi (Myoprocta pratti) with special reference to scatter hoarding. Proceed. Zool. Soc. Lond. 139, 701-732.
72. Odum, E. P. 1942 Annual cycle of the black-capped chickadee. Auk 59, 499-531.
73. O'Keefe, J. & Nadel, L. 1978 The hippocampus as a cognitive map. Oxford, UK: Clarendon Press.
74. Pravosudov, V. V. 1985 Search for and storage of food by Parus cinctus lapponicus and P montanus borealis (Paridae). Zool. Zh. 64, 1036-1043.
75. Pravosudov, V. V. 1986 Individual differences in the behavior of the Siberian tit (Parus cinctus Bodd.) and the willow tit (Parus montanus Bald.) in foraging and storing food. Sov. J. Ecol. 4, 237-241.
76. Pravosudov, V. V. & Clayton, N. S. 2002 A test of the adaptive specialization hypothesis: population differences in caching, memory, and the hippocampus in blackcapped chickadees (Poecile atricapilla). Behav. Neurosci. 116, 515-522. (doi:10.1037/0735-7044.116.4.515)
77. Price, M. V. & Mittler, J. M. 2003 Seed-cache exchange promotes coexistence and coupled consumer oscillations: a model of desert rodents as resource processors. J. Theor. Biol. 223, 215-231. (doi:10.1016/S0022-5193(03) 00088-2)
78. Price, M. V. & Mittler, J. M. 2006 Cachers, scavengers and thieves: a novel mechanism for desert rodent coexistence. Am. Nat. 168, 194-206. (doi: 10.1086/506277)
79. Roth, T. C. & Pravosudov, V. V. 2009 Hippocampal volume and neuron numbers increase along a gradient of environmental harshness: a large-scale comparison. Proc. R. Soc. B 276, 401-405. (doi:10.1098/rspb.2009.1184)
80. Roth II, T. C., Brodin, A., Smulders, T. V., LaDage, L. D. & Pravosudov, V. V. 2010 Is bigger always better? A critical appraisal of the use of volumetric analysis in the study of the hippocampus. Phil. Trans. R. Soc. B 365, 915-931. (doi: 10.1098/rstb.2009.0208)
81. Scoville, W. B. & Milner, B. 1957 Loss of recent memory after bilateral hippocampal lesions. J. Neurol. Neurosurg. Psychiatry 20, 11-21. (doi: 10.1136/jnnp.20.1.11)
82. Sherry, D. F. 1982 Food storage, memory, and marsh tits. Anim. Behav. 30, 631-633.
83. Sherry, D. F. 1984 Food storage by black-capped chickadees: memory for the location and contents of caches. Anim. Behav. 32, 451-464. (doi:10.1016/S0003-3472(84) 80281-X)
84. Sherry, D. F. 2006 Neuroecology. Annu. Rev. Psychol. 57, 167-197. (doi:10.1146/annurev.psych.56.091103. 070324)
85. Sherry, D. E. & Vaccarino, A. L. 1989 Hippocampus and memory for food caches in the black-capped chickadee. Behav. Neurosci. 103, 308-318. (doi: 10.1037/0735-7044.103.2.308)
86. Sherry, D. E., Krebs, J. R. & Cowie, R. J. 1981 Memory for the location of stored food in marsh tits. Anim. Behav. 29, 1260-1266. (doi:10.1016/S0003-3472(81)80078-4)
87. Sherry, D. F., Vaccarino, A. L., Buckenham, K. & Herz, R. S. 1989 The hippocampal complex of food-storing birds. Brain Behav. Evol. 34, 308-317. (doi:10.1159/ 000116516)
88. Shettleworth, S. J. 1995 Comparative studies of memory in food storing birds: from the field to the Skinner box. In Behavioral brain research in naturalistic and seminaturalistic settings (eds E. Alleva, A. Fasolo, H. P. Lipp, L. Nadel & L. Ricceri), pp. 169-192. Dordrecht, The Netherlands: Kluwer Academic Press.
89. Shettleworth, S. J. & Hampton, R. H. 1998 Adaptive specializations of spatial cognition in food storing birds? Approaches to testing a comparative hypothesis. In Animal cognition in nature (eds R. P. Balda, I. M. Pepperberg & A. C. Kamil), pp. 65-98. San Diego, CA: Academic Press.
90. Shettleworth, S. J. & Krebs, J. R. 1982 How marsh tits find their hoards: the roles of site preference and spatial memory. J. Exp. Psychol. Anim. Behav. Process. 8, 354-375. (doi:10.1037/0097-7403.8.4.354)
91. Shettleworth, S. J. & Krebs, J. R. 1986 Stored and encounterd seeds: a comparision of two spatial memory task in marsh tits and chickadees. J. Exp. Psychol. Anim. Behav. Process. 12, 248-257. (doi:10.1037/0097-7403.12.3.248)
92. Smulders, T. V. 1998 A game theoretical model of evolution of food hoarding: applications to the Paridae. Am. Nat. 151, 356-366. (doi: 10.1086/286124)
93. Smulders, T. V., Sasson, A. D. & DeVoogd, T. J. 1995 Seasonal variation in hippocampal volume in a food-storing bird, the black-capped chickadee. J. Neurobiol. 27, 15-25. (doi:10.1002/neu.480270103)
94. Stapanian, M. A. & Smith, C. C. 1978 A model for seed scatterhoarding: coevolution of fox squirrels and black walnuts. Ecology 59, 884-896. (doi:10.2307/1938541)
95. Stapanian, M. A. & Smith, C. C. 1984 Density-dependent survival of scatterhoarded nuts: an experimental approach. Ecology 65, 1387-1396. (doi:10.2307/1939119)
96. Stevens, T. A. & Krebs, J. R. 1985 Retrieval of stored seeds by marsh tits Parus palustris in the field. Ibis 128, 513-525. (doi:10.1111/j.l474-919X. 1986. tb02703.x)
97. Striedter, G. F. 2005 Principles of brain evolution. Sunderland, MA: Sinauer Associates.
98. Swanberg, P. O. 1951 Food storage, territory and song in the thick-billed nutcracker. In Proc. 10th Int. Ornithological Congress, pp. 545-554.
99. Swanberg, P. O. 1956 Territory in the thick-billed nutcracker Nucifraga caryocatactes. Ibis 98, 412-419. (doi:10.1111/ j.1474-919X.1956.tb01425.x)
100. Tinbergen, N. 1963 On aims and methods in ethology. Z. Tierpsychol. 20, 410-433.
101. Tinbergen, N. 1965 Von der Vorratskammern des rotfuchses (Wipes vulpes L.). Z. Tierpsychol. 22, 119-149.
102. Tinbergen, N., Impekoven, M. & Franck, D. 1967 An experiment on spacing-out as a defense against predation. Behaviour 28, 307-321. (doi:10.1163/ 156853967X00064)
103. Tomback, D. F. 1982 Dispersal of whitbark pine seeds by Clark's nutcracker: a mutualism hypothesis. J. Anim. Ecol. 51, 451-467.
104. Tomback, D. F. & Linhart, Y. B. 1990 The evolution of bird-dispersed pines. Evol. Ecol. 4, 185-219. (doi:10. 1007/BF02214330)
105. Vander Wall, S. B. 1982 An experimental analysis of cache recovery in Clark's nutcracker. Anim. Behav. 30, 84-94.
106. Vander Wall, S. B. 1990 Food hoarding in animals. Chicago, IL: Chicago University Press.
107. Vander Wall, S. B. 2010 How plants manipulate the scatterhoarding behaviour of seed-dispersing animals. Phil. Trans. R. Soc. B 365, 989-997. (doi:10.1098/rstb.2009. 0205)
108. Vander Wall, S. B. & Jenkins, S. H. 2003 Reciprocal pilferage and the evolution of food-hoarding behaviour. Behav. Ecol. 14, 656-667. (doi:10.1093/beheco/arg064)
109. Volman, S. F., Grubb, T. C. J. & Schuett, K. C. 1997 Relative hippocampal volume in relation to food-storing behavior in four species of Woodpeckers. Brain Behav. Evol. 49, 110-120. (doi: 10.1159/000112985)
110. von Pernau, J. F. A. 1720 von der Meise. In Angenehme Landlust, p. 226. Frankfurt: P. K. Monath.
111. Waite, T. A. 1990 Effects of caching supplemental food on induced feather regeneration in wintering gray jays Perisoreus canadensis: a ptilochronology study. Omis Scand. 21, 122-128. (doi: 10.2307/3676807)
112. Wauters, L. A., Suhonen, J. & Dhondt, A. A. 1995 Fitness consequences of hoarding behaviour in the Eurasian red squirrel. Proc. R. Soc. Lond. B 262, 277-281. (doi: 10. 1098/rspb.l995.0206)