Abstract
Directional climate change (global warming) is causing rapid alterations in animals’ environments. Because the nervous system is at the forefront of animals’ interactions with the environment, the neurobiological implications of climate change are central to understanding how individuals, and ultimately populations, will respond to global warming. Evidence is accumulating for individual level, mechanistic effects of climate change on nervous system development and performance. Climate change can also alter sensory stimuli, changing the effectiveness of sensory and cognitive systems for achieving biological fitness. At the population level, natural selection forces stemming from directional climate change may drive rapid evolutionary change in nervous system structure and function.
References
Aiello LC, Wheeler P (1995) The expensive-tissue hypothesis: the brain and the digestive system in human and primate evolution. Curr Anthropol 36(2):199–221. https://doi.org/10.1086/204350
Albright TP, Mutiibwa D, Gerson AR, Smith EK, Talbot WA, O’Neill JJ, McKechnie AE, Wolf BO (2017) Mapping evaporative water loss in desert passerines reveals an expanding threat of lethal dehydration. Proc Nat Acad Sci 114(9):2283–2288. https://doi.org/10.1073/pnas.1613625114
Amiel JJ, Bao S, Shine R (2017) The effects of incubation temperature on the development of the cortical forebrain in a lizard. Anim Cogn 20(1):117–125. https://doi.org/10.1007/s10071-016-0993-2
Aublet JF, Festa-Bianchet M, Bergero D, Bassano B (2009) Temperature constraints on foraging behaviour of male Alpine ibex (Capra ibex) in summer. Oecologia 159(1):237–247. https://doi.org/10.1007/s00442-008-1198-4
Avgar T, Mosser A, Brown GS, Fryxell JM (2013) Environmental and individual drivers of animal movement patterns across a wide geographical gradient. J Anim Ecol 82(1):96–106. https://doi.org/10.1111/j.1365-2656.2012.02035.x
Badeck FW, Bondeau A, Bottcher K, Doktor D, Lucht W, Schaber J, Sitch S (2004) Responses of spring phenology to climate change. New Phytol 162(2):295–309. https://doi.org/10.1111/j.1469-8137.2004.01059.x
Bartual A, Ortega MJ (2013) Temperature differentially affects the persistence of polyunsaturated aldehydes in seawater. Environ Chem 10(5):403–408. https://doi.org/10.1071/EN13055
Bautista DM, Siemens J, Glazer JM, Tsuruda PR, Basbaum AI, Stucky CL, Jordt SE, Julius D (2007) The menthol receptor TRPM8 is the principal detector of environmental cold. Nature 448(7150):204–208. https://doi.org/10.1038/nature05910
Berti R, Durand JP, Becchi S, Brizzi R, Keller N, Ruffat G (2001) Eye degeneration in the blind cave-dwelling fish Phreatichthys andruzzii. Can J Zool 79(7):1278–1285. https://doi.org/10.1139/z01-084
Bozinovic F, Portner HO (2015) Physiological ecology meets climate change. Ecol Evol 5(5):1025–1030. https://doi.org/10.1002/ece3.1403
Bradshaw WE, Holzapfel CM (2010) Light, time, and the physiology of biotic response to rapid climate change in animals. Annu Rev Physiol 72(1):147–166. https://doi.org/10.1146/annurev-physiol-021909-135837
Bulova S, Purce K, Khodak P, Sulger E, O’Donnell S (2016) Into the black and back: the ecology of brain investment in Neotropical army ants (Formicidae: Dorylinae). Sci Nat 103(3–4):31. https://doi.org/10.1007/s00114-016-1353-4
Calisi RM, Chintamen S, Ennin E, Kriegsfeld L, Rosenblum EB (2017) Neuroanatomical changes related to a changing environment in lesser earless lizards. J Herpetol 51(2):258–262. https://doi.org/10.1670/16-056
Catania KC (2000) Cortical organization in insectivora: the parallel evolution of the sensory periphery and the brain. Brain Behav Evol 55(6):311–321. https://doi.org/10.1159/000006666
Chen IC, Hill JK, Ohlemüller R et al (2011) Rapid range shifts of species associated with high levels of climate warming. Science 333(6045):1024–1026. https://doi.org/10.1126/science.1206432
Clapham DE (2003) TRP channels as cellular sensors. Nature 426(6966):517–524. https://doi.org/10.1038/nature02196
Clark TD, Roche DG, Binning SA, Ben Speers-Roesch B, Sundin J (2017) Maximum thermal limits of coral reef damselfishes are size dependent and resilient to near-future ocean acidification. J Exp Biol 220(19):3519–3526. https://doi.org/10.1242/jeb.162529
Cotton PA (2003) Avian migration phenology and global climate change. Proc Natl Acad Sci 100(21):12219–12222. https://doi.org/10.1073/pnas.1930548100
Cripps IL, Munday PL, McCormick MI (2011) Ocean acidification affects prey detection by a predatory reef fish. PLoS One 6(7):e22736. https://doi.org/10.1371/journal.pone.0022736
DeGregorio BA, Westervelt JD, Weatherhead PJ, Sperry JH (2015) Indirect effect of climate change: shifts in ratsnake behavior alter intensity and timing of avian nest predation. Ecol Model 312:239–246. https://doi.org/10.1016/j.ecolmodel.2015.05.031
Dhaka A, Viswanath V, Patapoutian A (2006) TRP ion channels and temperature sensation. Annu Rev Neurosci 29(1):135–161. https://doi.org/10.1146/annurev.neuro.29.051605.112958
Dixson DL, Jennings AR, Atema J, Munday PL (2015) Odor tracking in sharks is reduced under future ocean acidification conditions. Glob Chang Biol 21(4):1454–1462. https://doi.org/10.1111/gcb.12678
Doherty TJ, Clayton S (2011) The psychological impacts of global climate change. Am Psychol 66(4):265–276. https://doi.org/10.1037/a0023141
Esbaugh AJ (2017) Physiological implications of ocean acidification for marine fish: emerging patterns and new insights. J Comp Physiol B. https://doi.org/10.1007/s00360-017-1105-6
Fink P (2007) Ecological functions of volatile organic compounds in aquatic systems. Mar Freshw Behav Physiol 40(3):155–168. https://doi.org/10.1080/10236240701602218
Franks SJ, Hoffmann AA (2012) Genetics of climate change adaptation. Annu Rev Genet 46(1):185–208. https://doi.org/10.1146/annurev-genet-110711-155511
Gifford R (2011) The dragons of inaction: psychological barriers that limit climate change mitigation and adaptation. Am Psychol 66(4):290–302. https://doi.org/10.1037/a0023566
Gordo O (2007) Why are bird migration dates shifting? A review of weather and climate effects on avian migratory phenology. Clim Res 35:37–58. https://doi.org/10.3354/cr00713
Grant PR, Grant BR, Huey RB, Johnson MTJ, Knoll AH, Schmitt J (2017) Evolution caused by extreme events. Philos Trans R Soc B 372(1723):20160146. https://doi.org/10.1098/rstb.2016.0146
Groh C, Tautz J, Roessler W (2004) Synaptic organization in the adult honey-bee brain is influenced by brood-temperature control during pupal development. Proc Natl Acad Sci U S A 101(12):4268–4273. https://doi.org/10.1073/pnas.0400773101
Guerra PA, Reppert SM (2013) Coldness triggers northward flight in remigrant monarch butterflies. Curr Biol 23(5):419–423. https://doi.org/10.1016/j.cub.2013.01.052
Guerra PA, Reppert SM (2015) Sensory basis of lepidopteran migration: focus on the monarch butterfly. Curr Opin Neurobiol 34:20–28. https://doi.org/10.1016/j.conb.2015.01.009
Hamada FN, Rosenzweig M, Kang K, Pulver SR, Ghezzi A, Jegla TJ, Garrity PA (2008) An internal thermal sensor controlling temperature preference in Drosophila. Nature 454(7201):217–220. https://doi.org/10.1038/nature07001
Hamilton TJ, Holcombe A, Tresguerres M (2014) CO2 induced ocean acidification increases anxiety in Rockfish via alteration of GABA-A receptor functioning. Proc R Soc B 281:20132509
Hamilton SL, Logan CA, Fennie HW, Sogard SM, Barry JP, Makukhov AD, Tobosa LR, Boyer K, Lovera CF, Bernardi G (2017) Species-specific responses of juvenile rockfish to elevated pCO2: from behavior to genomics. PLoS One 12(1):e0169670. https://doi.org/10.1371/journal.pone.0169670
Herculano-Houzel S (2011) Scaling of brain metabolism with a fixed energy budget per neuron: implications for neuronal activity, plasticity and evolution. PloS One 6:e17514
Isler K, Van Schaik CP (2006) Metabolic costs of brain size evolution. Biol Lett 2(4):557–560. https://doi.org/10.1098/rsbl.2006.0538
Jeschke JM, Strayer DL (2008) Usefulness of bioclimatic models for studying climate change and invasive species. Ann N Y Acad Sci 1134(1):1–24. https://doi.org/10.1196/annals.1439.002
Kennedy AD (1997) Bridging the gap between general circulation model (GCM) output and biological microenvironments. Int J Biometeorol 40(2):119–122. https://doi.org/10.1007/s004840050031
Kinmonth-Schultz HA (2016) Determining day length and temperature regulation of flowering: a molecular and modelling approach. PhD dissertation, University of Washington, Seattle
Kotrschal A, Rogell B, Bundsen A, Svensson B, Zajitschek S, Brännström I, Immler S, Maklakov AA, Kolm N (2013) Artificial selection on relative brain size in the guppy reveals costs and benefits of evolving a larger brain. Curr Biol 23(2):168–171. https://doi.org/10.1016/j.cub.2012.11.058
LeGates TA, Fernandez DC, Hattar S (2014) Light as a central modulator of circadian rhythms, sleep and affect. Nat Rev Neurosci 15(7):443–454. https://doi.org/10.1038/nrn3743
Lopes AF, Morais P, Pimentel M, Rosa R, Munday PL, Goncalves EJ, Faria AM (2016) Behavioural lateralization and shoaling cohesion of fish larvae altered under ocean acidification. Mar Biol 163(12):243. https://doi.org/10.1007/s00227-016-3026-4
Maloney SK, Moss G, Cartmell T, Mitchell D (2005) Alteration in diel activity patterns as a thermoregulatory strategy in black wildebeest (Connochaetes gnou). J Comp Physiol A 191(11):1055–1064. https://doi.org/10.1007/s00359-005-0030-4
McKemy DD, Neuhausser WM, Julius D (2002) Identification of a cold receptor reveals a general role for TRP channels in thermosensation. Nature 416(6876):52–58. https://doi.org/10.1038/nature719
McLeman R, Smit B (2006) Migration as an adaptation to climate change. Clim Chang 76(1–2):31–53. https://doi.org/10.1007/s10584-005-9000-7
Mizoguchi H, Fukaya K, Mori R, Itoh M, Funakubo M, Sato J (2011) Lowering barometric pressure aggravates depression-like behavior in rats. Behav Brain Res 218(1):190–193. https://doi.org/10.1016/j.bbr.2010.11.057
Munday PL, Cheal AJ, Dixson DL, Rummer JL, Fabricius KE (2014) Behavioural impairment in reef fishes caused by ocean acidification at CO2 seeps. Nat Clim Chang 4(6):487–492. https://doi.org/10.1038/nclimate2195
Nams VO (2005) Using animal movement paths to measure response to spatial scale. Oecologia 143(2):179–188. https://doi.org/10.1007/s00442-004-1804-z
Nilsson GE, Dixson DL, Domenici P, McCormick MI, Sørensen C, Watson SA, Munday PL (2012) Near-future carbon dioxide levels alter fish behaviour by interfering with neurotransmitter function. Nat Clim Chang 2(3):201–204. https://doi.org/10.1038/nclimate1352
O’Donnell S, Clifford MR, Bulova SJ, DeLeon S, Papa C, Zahedi N (2014) A test of neuroecological predictions using paperwasp caste differences in brain structure (Hymenoptera: Vespidae). Behav Ecol Sociobiol 68(4):529–536. https://doi.org/10.1007/s00265-013-1667-6
Ou M, Hamilton TJ, Eom J, Lyall EM, Gallup J, Jiang A, Lee J, Close DA, Yun SS, Brauner CJ (2015) Responses of pink salmon to CO2-induced aquatic acidification. Nature. Clim Chang 5(10):950–955. https://doi.org/10.1038/nclimate2694
Pallotta MM, Turano M, Ronca R, Mezzasalma M, Petraccioli A, Odierna G, Capriglione T (2017) Brain gene expression is influenced by incubation temperature during leopard gecko (Eublepharis macularius) development. J Exp Zool 328B:360–370
Parmesan C (2006) Ecological and evolutionary responses to recent climate change. Ann Rev Ecol Evol Syst 37(1):637–669. https://doi.org/10.1146/annurev.ecolsys.37.091305.110100
Pounds JA, Fogden MP, Campbell JH (1999) Biological response to climate change on a tropical mountain. Nature 15:611–615
Pravosudov VV, Roth TC II, Forister ML et al (2013) Differential hippocampal gene expression is associated with climate-related natural variation in memory and the hippocampus in food-caching chickadees. Molec Ecol 22:397–408
Ramirez C, Nacher J, Molowny A, Sánchez-Sánchez F, Irurzun A, López-García C (1997) Photoperiod-temperature and neuroblast proliferation-migration in the adult lizard cortex. Neuroreport 8(9):2337–2442. https://doi.org/10.1097/00001756-199707070-00047
Reppert SM, Guerra PA, Merlin C (2016) Neurobiology of monarch butterfly migration. Annu Rev Entomol 61(1):25–42. https://doi.org/10.1146/annurev-ento-010814-020855
Robinson RA, Baillie SR, Crick HQ (2007) Weather-dependent survival: implications of climate change for passerine population processes. Ibis 149(2):357–364. https://doi.org/10.1111/j.1474-919X.2006.00648.x
Roth TC II, LaDage LD, Freas CA, Pravosudov VV (2012) Variation in memory and the hippocampus across populations from different climates: a common garden approach. Proc R Soc B 279:402–410
Roy M, Bouma M, Dhiman RC, Pascual M (2015) Predictability of epidemic malaria under non-stationary conditions with process-based models combining epidemiological updates and climate variability. Malar J 14(1):419. https://doi.org/10.1186/s12936-015-0937-3
Savoca MS, Nevitt GA (2014) Evidence that dimethyl sulfide facilitates a tritrophic mutualism between marine primary producers and top predators. Proc Nat Acad Sci 111(11):4157–4161. https://doi.org/10.1073/pnas.1317120111
Schloss CA, Nuñez TA, Lawler JJ (2012) Dispersal will limit ability of mammals to track climate change in the Western Hemisphere. Proc Nat Acad Sci 109(22):8606–8611. https://doi.org/10.1073/pnas.1116791109
Sherry DF (2006) Neuroecology. Ann Rev Psychol 57(1):167–197. https://doi.org/10.1146/annurev.psych.56.091103.070324
Shin LM, Rauch SL, Pittman RK (2006) Amygdala, medial prefrontal cortex, and hippocampal function in PTSD. Ann N Y Acad Sci 1071(1):67–79. https://doi.org/10.1196/annals.1364.007
Sibly RM, Calow P (1986) Physiological ecology of animals: an evolutionary approach. Blackwell Scientific Publications, Oxford, pp 179
Stevenson RD (1985) The relative importance of behavioral and physiological adjustments controlling body temperature in terrestrial ectotherms. Am Nat 126(3):362–386. https://doi.org/10.1086/284423
Sunday JM, Bates AE, Kearney MR, Colwell RK, Dulvy NK, Longino JT, Huey RB (2014) Thermal-safety margins and the necessity of thermoregulatory behavior across latitude and elevation. Proc Nat Acad Sci 111(15):5610–5615. https://doi.org/10.1073/pnas.1316145111
Tewksbury JJ, Huey RB, Deutsch CA (2008) Putting the heat on tropical animals. Science 320(5881):1296–1297. https://doi.org/10.1126/science.1159328
Todd BD, Scott DE, Pechmann JH et al (2011) Climate change correlates with rapid delays and advancements in reproductive timing in an amphibian community. Proc R Soc B 278(1715):2191–2197. https://doi.org/10.1098/rspb.2010.1768
Tresguerres M, Hamilton TJ (2017) Acid–base physiology, neurobiology and behaviour in relation to CO2-induced ocean acidification. J Exp Biol 220(12):2136–2148. https://doi.org/10.1242/jeb.144113
Urban MC, Zarnetske PL, Skelly DK (2013) Moving forward: dispersal and species interactions determine biotic responses to climate change. Ann N Y Acad Sci 1297:44–60. https://doi.org/10.1111/nyas.12184
Voets T, Droogmans G, Wissenbach U, Janssens A, Flockerzi V, Nilius B (2004) The principle of temperature-dependent gating in cold-and heat-sensitive TRP channels. Nature 430(7001):748–754. https://doi.org/10.1038/nature02732
Warren RJ II, Chick LD, DeMarco B et al (2016) Climate-driven range shift prompts species replacement. Insect Soc 63(4):593–601. https://doi.org/10.1007/s00040-016-0504-0
Welch KD, Harwood JD (2014) Temporal dynamics of natural enemy–pest interactions in a changing environment. Biol Control 75:18–27. https://doi.org/10.1016/j.biocontrol.2014.01.004
White (2015) States of emergency: trauma and climate change. Ecopsychology 7(4):192–197. https://doi.org/10.1089/eco.2015.0024
Wingfield JC (2008) Comparative endocrinology, environment and global change. Gen Comp Endocrinol 157(3):207–216. https://doi.org/10.1016/j.ygcen.2008.04.017
Wingfield JC (2015) Coping with change: a framework for environmental signals and how neuroendocrine pathways might respond. Front Neuroendocrinol 37:89–96. https://doi.org/10.1016/j.yfrne.2014.11.005
Acknowledgements
I thank five anonymous reviewers for making thoughtful and valuable comments on the manuscript.
Funding
Financial support was provided by Drexel University College of Arts and Sciences funds.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by: Sven Thatje
Rights and permissions
About this article
Cite this article
O’Donnell, S. The neurobiology of climate change. Sci Nat 105, 11 (2018). https://doi.org/10.1007/s00114-017-1538-5
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00114-017-1538-5