The three-way association among food-storing behavior, spatial memory, and hippocampal enlargement in some species of birds is widely cited as an example of a new ‘cognitive ecology’ or ‘neuroecology.’ Whether this relationship is as strong as it first appears and whether it might be evidence for an adaptive specialization of memory and hippocampus in food-storers have recently been the subject of some controversy [Bolhuis and Macphail, 2001; Macphail and Bolhuis, 2001]. These critiques are based on misconceptions about the nature of adaptive specializations in cognition, misconceptions about the uniformity of results to be expected from applying the comparative method to data from a wide range of species, and a narrow view of what kinds of cognitive adaptations are theoretically interesting. New analyses of why food-storers (black-capped chickadees, Poecile atricapilla) respond preferentially to spatial over color cues when both are relevant in a memory task show that this reflects a relative superiority of spatial memory as compared to memory for color rather than exceptional spatial attention or spatial discrimination ability. New studies of chickadees from more or less harsh winter climates also support the adaptive specialization hypothesis and suggest that within-species comparisons may be especially valuable for unraveling details of the relationships among ecology, memory, and brain in food-storing species.

Keywords:
Birds, Hippocampus, Spatial memory, Paridae, Food-storing, Black-capped chickadee, Dark-eyed junco
1.
Andersson M, Krebs J (1978) On the evolution of hoarding behaviour. Anim Behav 26:707–711.
2.
Balda RP, Kamil AC (1989) A comparative study of cache recovery by three corvid species. Anim Behav 38:486–495.
3.
Balda R, Kamil AC (2002) Spatial and social cognition in corvids: An evolutionary approach. In: The Cognitive Animal (Bekoff M, Allen C, Burghardt GM, eds), pp 129–134. Cambridge, MA: MIT Press.
4.
Barton RA, Harvey PH (2000) Mosaic evolution of brain structure in mammals. Nature 405:1055–1058.
5.
Basil JA, Kamil AC, Balda RP, Fite KV (1996) Differences in hippocampal volume among food storing corvids. Brain Behav Evol 47:156–164.
6.
Biegler R, McGregor A, Krebs JR, Healy SD (2001) A larger hippocampus is associated with longer-lasting spatial memory. Proc Natl Acad Sci USA 98:6941–6944.
7.
Bitterman ME (1975) The comparative analysis of learning. Science 188:699–709.
8.
Bitterman ME (2000) Cognitive evolution: A psychological perspective. In: The Evolution of Cognition (Heyes C, Huber L eds), pp 61–79. Cambridge MA: MIT Press.
9.
Bolhuis JJ, Macphail EM (2001) A critique of the neuroecology of learning and memory. Trends Cog Sci 5:426–433.
10.
Bolhuis JJ, Macphail EM (2002) Everything in neuroecology makes sense in the light of evolution. Trends Cog Sci 6:7–8.
11.
Brodbeck DR (1994) Memory for spatial and local cues: A comparison of a storing and a nonstoring species. Anim Learn Behav 22:119–133.
12.
Brodbeck DR, Shettleworth SJ (1995) Matching location and color of a compound stimulus: Comparison of a food-storing and a non-storing bird species. J Exp Psychol Anim Behav Process 21:64–77.
13.
Brodin A (1994) Separation of caches between individual willow tits hoarding under natural conditions. Anim Behav 47:1031–1035.
14.
Clayton NS (1996) Development of food-storing and the hippocampus in juvenile marsh tits (Parus palustris). Behav Brain Res 74:153–159.
15.
Clayton NS, Krebs JR (1994) Memory for spatial and object-specific cues in food-storing and non-storing birds. J Comp Physiol A 174:371–379.
16.
Colombo M, Broadbent N (2000) Is the avian hippocampus a functional homologue of the mammalian hippocampus? Neurosci Biobehav Rev 24:465–484.
17.
Domjan M (1980) Ingestional aversion learning: Unique and general processes. Adv Study Behav 11:275–336.
18.
Dwyer DM, Clayton NS (2002) A reply to the defenders of the faith. Trends Cog Sci 6:109–111.
19.
Ekman J, Brodin A, Bylin A, Sklepkovych B (1996) Selfish long-term benefits of hoarding in the Siberian jay. Behav Ecol 7:140–144.
20.
Haftorn S (1956) Contribution to the food biology of tits especially about storing of surplus food. Part IV. A comparative analysis of Parus atricapillus L., P. cristatus L. and P. ater L. Det Kgl Norske Videnskabers Selskabs Skrifter 1956 Nr 4:1–54.
21.
Hampton RR, Shettleworth SJ (1996a) Hippocampal lesions impair memory for location but not color in passerine birds. Behav Neurosci 110:831–835.
22.
Hampton RR, Shettleworth SJ (1996b) Hippocampus and memory in a food-storing and a non-storing bird species. Behav Neurosci 110:946–964.
23.
Hampton RR, Healy SD, Shettleworth SJ, Kamil AC (2002) Neuroecologists are not made of straw. Trends Cog Sci 6:6–7.
24.
Harvey PH, Krebs JR (1990) Comparing brains. Science 249:140–146.
25.
Harvey PH, Pagel D (1991) The Comparative Method in Evolutionary Biology. Oxford: Oxford University Press.
26.
Healy S, Braithwaite V (2000) Cognitive ecology: a field of substance? Trends Ecol Evol 15:22–26.
27.
Healy SD, Hurly TA (1998) Rufous hummingbirds’ (Selasphorus rufus) memory for flowers: Patterns or actual spatial locations? J Exp Psychol Anim Behav Proc 24:396–404.
28.
Kamil AC (1988) A synthetic approach to the study of animal intelligence. In: Comparative Perspectives in Modern Psychology: Nebraska Symposium on Motivation, Vol. 35 pp 230–257. Lincoln, NE: University of Nebraska Press.
29.
Kamil AC, Balda RP (1985) Cache recovery and spatial memory in Clark’s nutcrackers (Nucifraga columbiana) J Exp Psychol Anim Behav Proc 11:95–111.
30.
Kamil AC, Balda RP (1990) Spatial memory in seed-caching corvids. Psychol Learn Motiv 26:1–25.
31.
Krebs JR, Healy SD, Shettleworth SJ (1990) Spatial memory of Paridae: comparison of a storing and a non-storing species, the coal tit, Parus ater, and the great tit, P. major. Anim Behav 39:1127–1137.
32.
Krebs JR, Sherry DF, Healy SD, Perry VH, Vaccarino AL (1989) Hippocampal specialization of food-storing birds. Proc Natl Acad Sci USA 86:1388–1392.
33.
Lefebvre L (1996) Ecological correlates of social learning: problems and solutions for the comparative method. Behav Proc 35:163–171.
34.
Lefebvre L, Giraldeau L-A (1996) Is social learning an adaptive specialization? In: Social Learning in Animals: The Roots of Culture (Heyes CM, Galef BG eds), pp 107–128. San Diego, CA: Academic Press.
35.
MacDougall-Shackleton SA, Ball GF (1999) Comparative study of sex differences in the song-control system of songbirds. Trends Neurosci 22:432–436.
36.
MacDougall-Shackleton SA, Ball GF (2002) Revising hypotheses does not indicate a flawed approach. Trends Cog Sci 6:68–69.
37.
Macphail EM (1987) The comparative psychology of intelligence. Behav Brain Sci 10:645–695.
38.
MacPhail EM (2002) The role of the avian hippocampus in spatial memory. Psicologia 23:93–108.
39.
Macphail EM, Bolhuis JJ (2001) The evolution of intelligence: adaptive specialisations versus general process. Biol Rev 76:341–364.
40.
McGregor A, Healy SD (1999) Spatial accuracy in food-storing and nonstoring birds. Anim Behav 58:727–734.
41.
Nilsson J-A, Kallander H, Persson O (1993) A prudent hoarder: effects of long-term hoarding in the European nuthatch, Sitta europaea. Behav Ecol 4:369–373.
42.
Papini M (2002) Pattern and process in the evolution of learning. Psychol Rev 109:186–201.
43.
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.
44.
Plotkin H (1997) Evolution of Mind. London: The Penguin Press.
45.
Pravosudov VV, Clayton NS (2002) A test of the adaptive specialization hypothesis: Population differences in caching, memory, and the hippocampus in black-capped chickadees (Poscile atricapilla). Behav Neurosci 116:515–522.
46.
Raff RA (1996). The Shape of Life. Chicago: University of Chicago Press.
47.
Reboreda JC, Clayton NS, Kacelnik A (1996) Species and sex differences in hippocampus size in parasitic and non-parasitic cowbirds. Neuroreport 7:505–508.
48.
Rozin P, Kalat JW (1971) Specific hungers and poison avoidance as adaptive specializations of learning. Psychol Rev 78:459–486.
49.
Sherry DF, Duff SJ (1996) Behavioural and neural bases of orientation in food-storing birds. J Exp Biol 199:165–172.
50.
Sherry DF, Schacter DL (1987) The evolution of multiple memory systems. Psychol Rev 94:439–454.
51.
Sherry D, Vaccarino AL (1989) Hippocampus and memory for food caches in black-capped chickadees. Behav Neurosci 103:308–318.
52.
Sherry DF, Jacobs LF, Gaulin SJC (1992) Spatial memory and adaptive specialization of the hippocampus. Trends Neurosci 15:298–303.
53.
Sherry D, Krebs JR, Cowie RJ (1981) Memory for the location of stored food in marsh tits. Anim Behav 29:1260–1266.
54.
Sherry D, Vaccarino AL, Buckenham K, Herz RS (1989) The hippocampal complex of food-storing birds. Brain Behav Evol 34:308–317.
55.
Shettleworth SJ (1995) Comparative studies of memory in food storing birds: From the field to the Skinner box. In: Behavioral Brain Research in Naturalistic and Semi-Naturalistic Settings (Alleva E, Fasolo A, Lipp HP, Nadel L, Ricceri L, eds) pp 169–192. Dordrecht: Kluwer Academic Press.
56.
Shettleworth SJ (1998) Cognition, Evolution, and Behavior. New York: Oxford University Press.
57.
Shettleworth SJ (2000) Modularity and the evolution of cognition. In: The Evolution of Cognition (Heyes C, Huber L, eds) pp 43–60. Cambridge MA: MIT Press.
58.
Shettleworth SJ, Hampton RH (1998) Adaptive specializations of spatial cognition in food storing birds? Approaches to testing a comparative hypothesis. In: Animal Cognition in Nature (Balda RP, Pepperberg IM, Kamil AC, eds) pp 65–98. San Diego: Academic Press.
59.
Shettleworth SJ, Westwood RP (2002) Divided attention, memory, and spatial discrimination in food-storing and non-storing birds, black-capped chickadees (Poecile atricapilla) and dark-eyed juncos (Junco hyemalis). J Exp Psychol Anim Behav Proc 28:227–241.
60.
Strasser R, Bingman VP (1996) The relative importance of location and feature cues for homing pigeon (Columba livia) goal recognition. J Comp Psychol 110:77–87.
61.
Tinbergen N (1963) On aims and methods of ethology. Zeitschr Tierpsychol 20:410–433.
62.
Vander Wall SB (1982) An experimental analysis of cache recovery in Clark’s nutcracker. Anim Behav 30:84–94.
63.
Vander Wall SB (1990). Food Hoarding in Animals. Chicago: University of Chicago Press.
64.
Vander Wall SB, Balda RP (1981) Ecology and evolution of food-storage behavior in conifer-seed -caching corvids. Zeitschr Tierpsychol 56:217–242.
65.
Wasserman EA (1993) Comparative cognition: Beginning the second century of the study of animal intelligence. Psychol Bull 113:211–228.
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