Abstract
Environmental conditions may provide specific demands for memory, which in turn may affect specific brain regions responsible for memory function. For food-caching animals, in particular, spatial memory appears to be important because it may have a direct effect on fitness via the accuracy of cache retrieval. Animals living in more harsh environments should rely more on cached food, and thus theoretically should have better memory to support cache retrieval, which may be crucial for survival. Consequently, animals in harsh environments may benefit from more neurons within a larger hippocampus (Hp), a part of the brain involved in spatial memory. Here, we present the first large-scale test of the hypothesis that Hp structure is related to the severity of the environment within a single food-caching species (the black-capped chickadee, Poecile atricapillus) with a large range encompassing a great diversity of climatic conditions. Hp size in birds collected at five locations along a gradient of environmental harshness from Alaska to Kansas ranked perfectly with climatic severity. Birds from more harsh northern climates (defined by lower ambient temperature, shorter day length and more snow cover) had significantly larger Hp volumes and more Hp neurons (both relative to telencephalon volume) than those from more mild southern latitudes. Environmental pressures therefore seem capable of influencing specific brain regions independently, which may result in enhanced memory, and hence survival, in harsh climates.
References
-
Bolhuis J.J& Macphail E.M . 2001 A critique of the neuroecology of learning and memory. Trends Cogn. Sci. 4, 426–433.doi:10.1016/S1364-6613(00)01753-8. . Crossref, ISI, Google Scholar -
Brodin A . 2005 Hippocampal volume does not correlate with food-hoarding rates in the black-capped chickadee and willow tit. Auk. 122, 819–828.doi:10.1642/0004-8038(2005)122[0819:HVDNCW]2.0.CO;2. . Crossref, ISI, Google Scholar -
Brodin A& Bolhuis J.J . 2008 Memory and brain in food storing birds: space oddities or adaptive specialisations?. Ethology. 114, 633–645.doi:10.1111/j.1439-0310.2008.01508.x. . Crossref, ISI, Google Scholar -
Brodin A& Lundborg K . 2003 Is hippocampal volume affected by specialization for food hoarding in birds?. Proc. R. Soc. B. 270, 1555–1563.doi:10.1098/rspb.2003.2413. . Link, ISI, Google Scholar -
de Kort S.R& Clayton N.S . 2006 An evolutionary perspective on caching by corvids. Proc. R. Soc. B. 273, 417–423.doi:10.1098/rspb.2005.3350. . Link, ISI, Google Scholar -
Environment Canada 2008 Climate data 1971–2000. See http://www.climate.weatheroffice.ec.gc.ca. Google Scholar
-
Gaines S.D& Rice R.R . 1990 Analysis of biological data when there are ordered expectations. Am. Nat. 135, 310–317.doi:10.1086/285047. . Crossref, ISI, Google Scholar -
Garamszegi L.Z& Eens M . 2004 The evolution of hippocampus volume and brain size in relation to food hoarding in birds. Ecol. Lett. 7, 1216–1224.doi:10.1111/j.1461-0248.2004.00685.x. . Crossref, ISI, Google Scholar -
Gundersen H.J.G& Jensen E.B . 1987 The efficiency of systematic sampling in stereology and its prediction. J. Microsc. Oxf. 147, 229–263. Crossref, PubMed, ISI, Google Scholar -
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. . Crossref, PubMed, ISI, Google Scholar -
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. 86, 1388–1392.doi:10.1073/pnas.86.4.1388. . Crossref, PubMed, ISI, Google Scholar -
Lucas J.R, Brodin A, de Kort S.R& Clayton N.S . 2004 Does hippocampal size correlate with the degree of caching specialization?. Proc. R. Soc. B. 271, 2423–2429.doi:10.1098/rspb.2004.2912. . Link, ISI, Google Scholar -
Macphail E.M& Bolhuis J.J . 2001 The evolution of intelligence: adaptive specializations versus general process. Biol. Rev. 76, 341–364.doi:10.1017/S146479310100570X. . Crossref, PubMed, ISI, Google Scholar -
National Oceanic and Atmospheric Administration 2008 Climate data 1971–2000. See http://www.weather.gov/climate. Google Scholar
-
Pravosudov V.V . 2006 On seasonality in food-storing behaviour in parids: do we know the whole story?. Anim. Behav. 71, 1455–1460.doi:10.1016/j.anbehav.2006.01.006. . Crossref, ISI, Google Scholar -
Pravosudov V.V& Clayton N.S . 2002 A test of the adaptive specialization hypothesis: population differences in caching, memory, and the hippocampus in black-capped chickadees (Poecile atricapilla). Behav. Neurosci. 116, 515–522.doi:10.1037/0735-7044.116.4.515. . Crossref, PubMed, ISI, Google Scholar -
Pravosudov V.V& Grubb T.C . 1997 Management of fat reserves and food caches in tufted titmice (Parus bicolor) in relation to unpredictable food supply. Behav. Ecol. 8, 332–339.doi:10.1093/beheco/8.3.332. . Crossref, ISI, Google Scholar -
Pravosudov V.V& Lucas J.R . 2001 A dynamic model of short-term energy management in small food-caching and non-caching birds. Behav. Ecol. 12, 207–218.doi:10.1093/beheco/12.2.207. . Crossref, ISI, Google Scholar -
Pravosudov V.V& Omanska A . 2005 Dominance-related changes in spatial memory are associated with changes in hippocampal cell proliferation rates in mountain chickadees. J. Neurobiol. 62, 31–41.doi:10.1002/neu.20065. . Crossref, PubMed, Google Scholar -
Rice R.R& Gaines S.D . 1994 The ordered-heterogeneity family of tests. Biometrics. 50, 746–752.doi:10.2307/2532788. . Crossref, ISI, Google Scholar -
Roth G& Dicke U . 2005 Evolution of the brain and intelligence. Trends Cogn. Sci. 9, 250–257.doi:10.1016/j.tics.2005.03.005. . Crossref, PubMed, ISI, Google Scholar -
Sherry D.F& Vaccarino A.L . 1989 Hippocampus and memory for food caches in black-capped chickadees. Behav. Neurosci. 103, 308–318.doi:10.1037/0735-7044.103.2.308. . Crossref, ISI, Google Scholar -
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. . Crossref, PubMed, ISI, Google Scholar -
Sherry D.F, Jacobs L.F& Gaulin S.J.C . 1992 Spatial memory and adaptive specialization of the hippocampus. Trends Neurosci. 15, 298–303.doi:10.1016/0166-2236(92)90080-R. . Crossref, PubMed, ISI, Google Scholar -
Shettleworth S.J Memory in food-storing birds: from the field to the skinner box. Behavioral brain research in naturalistic and semi-naturalistic settings, Alleva E, Fasolo A, Lipp H.P, Nadel L& Ricceri L . 1995pp. 158–179. Eds. The Hague, The Netherlands:Kluwer. Google Scholar -
Shettleworth S.J Cognition, evolution, and behavior. 1998 Oxford, UK:Oxford University Press. Google Scholar -
Vander Wall S.B Food hoarding in animals. 1990 Chicago, IL:University of Chicago Press. Google Scholar -
West M.J, Slomianka L& Gundersen H.J.G . 1991 Unbiased stereological estimation of the total number of neurons in the subdivisions of the rat hippocampus using the optical fractionator. Anat. Rec. 231, 482–497.doi:10.1002/ar.1092310411. . Crossref, PubMed, Google Scholar