487
Views
16
Downloads
23
Crossref
N/A
WoS
26
Scopus
0
CSCD
Brain size may affect the probability of invasion of urban habitats if a relatively larger brain entails superior ability to adapt to novel environments. However, once urbanized urban environments may provide poor quality food that has negative consequences for normal brain development resulting in an excess of individuals with small brains.
Here we analyze the independent effects of mean, standard deviation and skewness in brain mass for invasion of urban habitats by 108 species of birds using phylogenetic multiple regression analyses weighted by sample size.
There was no significant difference in mean brain mass between urbanized and non-urbanized species or between urban and rural populations of the same species, and mean brain mass was not significantly correlated with time since urbanization. Bird species that became urbanized had a greater standard deviation in brain mass than non-urbanized species, and the standard deviation in brain mass increased with time since urbanization. Brain mass was significantly left skewed in species that remained rural, while there was no significant skew in urbanized species. The degree of left skew was greater in urban than in rural populations of the same species, and successfully urbanized species decreased the degree of left skew with time since urbanization. This is consistent with the hypothesis that sub-optimal brain development was more common in rural habitats resulting in disproportionately many individuals with very small brains.
These findings do not support the hypothesis that large brains promote urbanization, but suggest that skewness has played a role in the initial invasion of urban habitats, and that variance and skew in brain mass have increased as species have become urbanized.
Brain size may affect the probability of invasion of urban habitats if a relatively larger brain entails superior ability to adapt to novel environments. However, once urbanized urban environments may provide poor quality food that has negative consequences for normal brain development resulting in an excess of individuals with small brains.
Here we analyze the independent effects of mean, standard deviation and skewness in brain mass for invasion of urban habitats by 108 species of birds using phylogenetic multiple regression analyses weighted by sample size.
There was no significant difference in mean brain mass between urbanized and non-urbanized species or between urban and rural populations of the same species, and mean brain mass was not significantly correlated with time since urbanization. Bird species that became urbanized had a greater standard deviation in brain mass than non-urbanized species, and the standard deviation in brain mass increased with time since urbanization. Brain mass was significantly left skewed in species that remained rural, while there was no significant skew in urbanized species. The degree of left skew was greater in urban than in rural populations of the same species, and successfully urbanized species decreased the degree of left skew with time since urbanization. This is consistent with the hypothesis that sub-optimal brain development was more common in rural habitats resulting in disproportionately many individuals with very small brains.
These findings do not support the hypothesis that large brains promote urbanization, but suggest that skewness has played a role in the initial invasion of urban habitats, and that variance and skew in brain mass have increased as species have become urbanized.
Almond D, Edlund L, Palmer M (2007) Chernobyl's subclinical legacy: Prenatal exposure to radioactive fallout and school outcomes in Sweden. Natl Bureau Econ Res 13347:1-50
Armstrong E, Bergeron R (1985) Relative brain size and metabolism in birds. Brain Behav Evol 26:141-153
Bains JS, Shaw CA (1997) Neurodegenerative disorders in humans: The role of glutathione in oxidative stress-mediated neuronal death. Brain Res Rev 25:335-358
Baratti M, Cordaro M, Dessi-Fulgheri F, Vannini M, Fratini S (2009) Molecular and ecological characterization of urban populations of the mallard (Anas platyrhynchos) in Italy. Ital J Zool 76:330-339
Björklund M, Ruiz I, Senar JC (2010) Genetic differentiation in the urban habitat: The great tits (Parus major) of the parks of Barcelona city. Biol J Linn Soc 99:9-19
Bonaparte KM, Riffle-Yokoi C, Burley NT (2011) Getting a head start: Diet, sub-adult growth, and associative learning in a seed-eating passerine. PLoS One 6(9):e23775
Carrete M, Tella JL (2011) Inter-individual variability in fear of humans and relative brain size of the species are related to contemporary urban invasion in birds. PLoS One 6(4):e18859
Crile G, Quiring DP (1940) A record of the body weight and certain organ and gland weight of 3690 animals. Ohio J Sci 40:219-259
Croci S, Butet A, Clergeau P (2008) Does urbanization filter birds on the basis of their biological traits? Condor 110:223-240
Evans KL, Gaston KJ, Frantz AC, Simeoni M, Sharp SP, McGowan A, Dawson DA, Walasz K, Partecke J, Burke T, Hatchwell BJ (2009) Independent colonization of multiple urban centres by a formerly forest specialist bird species. Proc R Soc Lond B 276:2403-2410
Evans KL, Chamberlain DE, Hatchwell BJ, Gregory RD, Gaston KJ (2011) What makes an urban bird? Global Change Biol 17:32-44
Fulgione D, Rippa D, Procaccini G, Milone M (2000) Urbanisation and the genetic structure of Passer italiae (Viellot 1817) populations in the south of Italy. Ethol Ecol Evol 12:123-130
Garamszegi LZ, Møller AP (2010) Effects of sample size and intraspecific variation in phylogenetic comparative studies: A meta-analytic review. Biol Rev 85:797-805
Gliwicz J, Goszczynski J, Luniak M (1994) Characteristic features of animal populations under synurbanization: The case of the Blackbirds and the striped field mouse. Mem Zool 49:237-244
Harvey PH, Pagel M (1991) The Comparative Method in Evolutionary Biology. Oxford University Press, Oxford, UK
Heiervang KS, Mednick S, Sundet K, Rund BR (2010) Effect of low dose ionizing radiation exposure in utero on cognitive function in adolescence. Scand J Psychol 51:210-215
Hoffman DJ, Heinz GH (1998) Effects of mercury and selenium on glutathione metabolism and oxidative stress in mallard ducks. Environ Toxicol Chem 17:161-166
Kark S, Iwaniuk A, Schalimtzek A, Banker E (2007) Living in the city: Can anyone become an 'urban exploiter'? J Biogeogr 34:638-651
Laughlin SB (2001) Energy as a constraint on the coding and processing of sensory information. Curr Opin Neurobiol 11:475-480
Laughlin SB, van Steveninck RRD, Anderson JC (1998) The metabolic cost of neural information. Nat Neurosci 1:36-41
Maklakov AA, Immler S, Gonzalez-Voyer A, Rönn J, Kolm N (2011) Brains and the city: Big-brained passerine birds succeed in urban environments. Biol Lett 7:730-732
Mlikovsky J (1990) Brain size in birds: 4. Passeriformes. Acta Soc Zool Bohemoslov 54:27-37
Møller AP (2008) Flight distance of urban birds, predation and selection for urban life. Behav Ecol Sociobiol 63:63-75
Møller AP (2009) Successful city dwellers: A comparative study of the ecological characteristics of urban birds in the Western Palearctic. Oecologia 159:849-858
Møller AP (2010) Interspecific variation in fear responses predicts urbanization in birds. Behav Ecol 21:365-371
Møller AP, Nielsen JT (2007) Malaria and risk of predation: A comparative study of birds. Ecology 88:871-881
Møller AP, Surai PF, Mousseau TA (2005) Antioxidants, radiation and mutation in barn swallows from Chernobyl. Proc R Soc Lond B 272:247-253
Møller AP, Erritzøe J, Karadas F (2010) Levels of antioxidants in rural and urban birds and their consequences. Oecologia 163:35-45
Møller AP, Bonisoli-Alquati A, Rudolfsen G, Mousseau TA (2011) Chernobyl birds have smaller brains. PLoS One 6(2):e16862
Møller AP, Diaz M, Flensted-Jensen E, Grim T, Ibáñez-Álamo JD, Jokimäki J, Mänd R, Marko G, Tryjanowski P (2012) High urban population density of birds reflects their timing of urbanization. Oecologia 170:867-875
Nilsson GE (1999) Brain and body oxygen requirements of Gnathonemus petersii, a fish with an exceptionally large brain. J Exp Biol 199:603-607
Purvis A, Rambaut A (1995) Comparative analysis by independent contrasts (CAIC): an Apple-Macintosh application for analyzing comparative data. Comput Appl Biosci 11:247-251
Ricklefs RE (2004) The cognitive face of avian life histories. Wilson Bull 116:119-133
Rutkowski R, Rejt L, Gryczynska-Siematkowska A, Jagolkowska P (2005) Urbanization gradient and genetic variability of birds: Example of kestrels in Warsaw. Berkut 14:130-136
Sewalk CJ, Brewer GL, Hoffman DJ (2001) Effects of diquat, an aquatic herbicide, on the development of mallard embryos. J Toxicol Environ Health A 62:33-45
Sol D, Lefebvre L (2000) Behavioural flexibility predicts invasion success in birds introduced to New Zealand. Oikos 90:599-605
Sol D, Timmermans S, Lefebvre L (2002) Behavioural flexibility and invasion success in birds. Anim Behav 63:495-502
Sol D, Duncan RP, Blackburn TM, Cassey P, Lefebvre L (2005) Big brains, enhanced cognition, and response of birds to novel environments. Proc Natl Acad Sci U S A 102:5460-5465
This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.