Feeling the cold in a warming climate: differential effects of low temperatures on co-occurring eucalypts
George Matusick A B C , Katinka X. Ruthrof A , Jason Pitman A and Giles E. St. J. Hardy A
+ Author Affiliations
- Author Affiliations
A School of Veterinary and Life Sciences, Murdoch University, WA 6150, Australia.
B Present address: The Nature Conservancy, Georgia Chapter, Chattahoochee Fall Line Project, Fort Benning, Georgia, 31905, United States.
C Corresponding author. Email: G.Matusick@murdoch.edu.au
Australian Journal of Botany 64(5) 456-466 https://doi.org/10.1071/BT16064
Submitted: 1 April 2016 Accepted: 13 July 2016 Published: 29 July 2016
Abstract
Climate change is altering extreme temperature events, and is expected to drive changes in species composition as a result. To assess the potential for compositional shifts from low-temperature events, the effects of repeated events in 2010 and 2012 on three co-occurring eucalypts were determined in south-western Australia. To examine the climatic conditions that led to tree damage, and the long-term pattern of low-temperature events, temperatures were monitored on affected sites, and modelled from climate-station data. The three species varied considerably in their susceptibility to low temperatures. Corymbia calophylla K.D.Hill & L.A.S.Johnson was most affected (crown-damage index (CDI) = 47), followed by Eucalyptus marginata Sm. (CDI = 17) and E. wandoo Blakely (CDI = 3), which was comparatively tolerant. The temperatures leading to damage in 2010 and 2012 were –3.4°C and –2.1°C respectively. The frequency of low-temperature events (days below 0°C) have been steadily increasing in the study area since the mid-1990s. Because minimal tree mortality was observed, species composition is unlikely to change as a result of low temperatures in the short term. However, continued dieback from repeated events may disrupt regenerative processes, and cause long-term compositional shifts.
Additional keywords: climate change, eucalypt dieback, Eucalyptus, forest ecology, frost, jarrah.
References
Allen DC, Barnett CJ, Millers I, Lachance D (1992) Temporal change (1988–1990) in sugar maple health, and factors associated with crown condition. Canadian Journal of Forest Research 22, 1776–1784.| Temporal change (1988–1990) in sugar maple health, and factors associated with crown condition.Crossref | GoogleScholarGoogle Scholar |
Allen CD, Macalady AK, Chenchouni H, Bachelet D, McDowell N, Vennetier M, Kitzberger T, Rigling A, Breshears DD, Hogg EH, Gonzalez P, Fensham R, Zhang Z, Castro J, Demidova N, Lim J-H, Allard G, Running SW, Semerci A, Cobb N (2010) A global overview of drought and heat-induced tree mortality reveals emerging climate change risks for forests. Forest Ecology and Management 259, 660–684.
| A global overview of drought and heat-induced tree mortality reveals emerging climate change risks for forests.Crossref | GoogleScholarGoogle Scholar |
Anandhi A, Perumal S, Gowda PH, Knapp M, Hutchinson S, Harrington J, Murray L, Kirkham MB, Rice CW (2013) Long-term spatial and temporal trends in frost indices in Kansas, USA. Climatic Change 120, 169–181.
| Long-term spatial and temporal trends in frost indices in Kansas, USA.Crossref | GoogleScholarGoogle Scholar |
Anderegg WRL, Kane JM, Anderegg LDL (2012) Consequences of widespread tree mortality triggered by drought and temperature stress. Nature Climate Change 3, 30–36.
| Consequences of widespread tree mortality triggered by drought and temperature stress.Crossref | GoogleScholarGoogle Scholar |
Ashton DH (1958) The ecology of Eucalyptus regnans F.Muell.: the species and its frost resistance. Australian Journal of Botany 6, 154–176.
| The ecology of Eucalyptus regnans F.Muell.: the species and its frost resistance.Crossref | GoogleScholarGoogle Scholar |
Augspurger CK (2009) Spring 2007 warmth and frost: phenology, damage and refoliation in a temperature deciduous forest. Functional Ecology 23, 1031–1039.
| Spring 2007 warmth and frost: phenology, damage and refoliation in a temperature deciduous forest.Crossref | GoogleScholarGoogle Scholar |
Augspurger CK (2011) Frost damage and its cascading negative effects on Aesculus glabra. Plant Ecology 212, 1193–1203.
| Frost damage and its cascading negative effects on Aesculus glabra.Crossref | GoogleScholarGoogle Scholar |
Augspurger CK (2013) Reconstructing patterns of temperature, phenology, and frost damage over 124 years: Spring damage risk is increasing. Ecology 94, 41–50.
| Reconstructing patterns of temperature, phenology, and frost damage over 124 years: Spring damage risk is increasing.Crossref | GoogleScholarGoogle Scholar | 23600239PubMed |
Barker DH, Loveys BR, Egerton JJG, Gorton H, Williams WE, Ball MCB (2005) CO2 enrichment predisposes foliage of a eucalypt to freezing injury and reduces spring growth. Plant, Cell & Environment 28, 1506–1515.
| CO2 enrichment predisposes foliage of a eucalypt to freezing injury and reduces spring growth.Crossref | GoogleScholarGoogle Scholar |
Bates BC, Hope P, Ryan B, Smith I, Charles S (2008) Key findings from the Indian Ocean Climate Initiative and their impact on policy development in Australia. Climatic Change 89, 339–354.
| Key findings from the Indian Ocean Climate Initiative and their impact on policy development in Australia.Crossref | GoogleScholarGoogle Scholar |
Batini F (2007) The response of Australian forests to a drying climate: a case study of the jarrah forest. Australian Forestry 70, 213–214.
Bell DT, Heddle EM (1989) Floristic, morphology, and vegetational diversity. In ‘The jarrah forest: a complex Mediterranean ecosystem’. (Eds B Dell, JJ Havel, N Malajczuk) pp. 53–66. (Kluwer Academic Publishers: Dordrecht, The Nethelands)
Breshears DD, Cobb NS, Rich PM, Price KP, Allen CD, Balice RG, Romme WH, Kastens JD, Floyd ML, Belnap J, Anderson JJ, Myers OB, Meyer CW (2005) Regional vegetation die-off in response to global-change-type drought. Proceedings of the National Academy of Sciences, USA 102, 15144–15148.
| Regional vegetation die-off in response to global-change-type drought.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtFGqtb3I&md5=feb46192effeee155f24b6a261f34feeCAS |
Brouwers N, Matusick G, Ruthrof K, Lyons T, Hardy G (2013) Landscape-scale assessment of tree crown dieback following extreme drought and heat in a Mediterranean eucalypt forest ecosystem. Landscape Ecology 28, 69–80.
| Landscape-scale assessment of tree crown dieback following extreme drought and heat in a Mediterranean eucalypt forest ecosystem.Crossref | GoogleScholarGoogle Scholar |
Burrows N, Gardiner G, Ward B, Robinson A (1990) Regeneration of Eucalyptus wandoo following fire. Australian Forestry 53, 248–258.
| Regeneration of Eucalyptus wandoo following fire.Crossref | GoogleScholarGoogle Scholar |
Byrne M, Murrell JC, Owen JV, Williams ER, Moran GF (1997) Mapping quantitative trait loci influencing frost tolerance in Eucalyptus nitens. Theoretical and Applied Genetics 95, 975–979.
| Mapping quantitative trait loci influencing frost tolerance in Eucalyptus nitens.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXns1OrsLs%3D&md5=b0ed6a68ddeb5b85a50542d52355d02eCAS |
Cavin L, Mountford EP, Peterken GF, Jump AS (2013) Extreme drought alters competitive dominance within and between tree species in a mixed forest stand. Functional Ecology 27, 1424–1435.
| Extreme drought alters competitive dominance within and between tree species in a mixed forest stand.Crossref | GoogleScholarGoogle Scholar |
Churchward HM, Dimmock GM (1989) The soils and landforms of the northern jarrah forest. In ‘The jarrah forest: a complex Mediterranean ecosystem’. (Eds B Dell, JJ Havel, N Malajczuk) pp. 13–21. (Kluwer Academic Publishers: Dordrecht, The Netherlands)
Clark JS, Melillo J, Mohan J, Salk C (2014) The seasonal timing of warming that controls onset of the growing season. Global Change Biology 20, 1136–1145.
| The seasonal timing of warming that controls onset of the growing season.Crossref | GoogleScholarGoogle Scholar | 24115181PubMed |
Climent J, Silva FCE, Chambel MR, Pardos M, Almeida MH (2009) Freezing injury in primary and secondary needles of Mediterranean pine species of contrasting niches. Annals of Forest Science 66, 407–415.
| Freezing injury in primary and secondary needles of Mediterranean pine species of contrasting niches.Crossref | GoogleScholarGoogle Scholar |
Daly C, Conklin DR, Unsworth MH (2010) Local atmospheric decoupling in complex topography alters climate change impacts. International Journal of Climatology 30, 1857–1864.
| Local atmospheric decoupling in complex topography alters climate change impacts.Crossref | GoogleScholarGoogle Scholar |
Davidson NJ, Reid JB (1985) Frost as a factor influencing the growth and distribution of subalpine eucalypts. Australian Journal of Botany 33, 657–667.
| Frost as a factor influencing the growth and distribution of subalpine eucalypts.Crossref | GoogleScholarGoogle Scholar |
Davidson NJ, Reid JB (1987) The influence of hardening and waterlogging on the frost resistance of subalpine eucalypts. Australian Journal of Botany 35, 91–101.
| The influence of hardening and waterlogging on the frost resistance of subalpine eucalypts.Crossref | GoogleScholarGoogle Scholar |
Diffenbaugh NS, Pal JS, Giorgi F, Gao X (2007) Heat stress intensification in the Mediterranean climate change hotspot. Geophysical Research Letters 34, L11706
| Heat stress intensification in the Mediterranean climate change hotspot.Crossref | GoogleScholarGoogle Scholar |
Erlat E, Türkes M (2012) Analysis of observed variability and trends in numbers of frost days in Turkey for the period 1950–2010. International Journal of Climatology 32, 1889–1898.
| Analysis of observed variability and trends in numbers of frost days in Turkey for the period 1950–2010.Crossref | GoogleScholarGoogle Scholar |
Espírito Santo FE, de Lima MIP, Ramos AM, Trigo RM (2014) Trends in seasonal surface air temperature in mainland Portugal, since 1941. International Journal of Climatology 34, 1814–1837.
| Trends in seasonal surface air temperature in mainland Portugal, since 1941.Crossref | GoogleScholarGoogle Scholar |
Fensham R, Holman JE (1999) Temporal and spatial patterns in drought-related tree dieback in Australian savanna. Journal of Applied Ecology 36, 1035–1050.
| Temporal and spatial patterns in drought-related tree dieback in Australian savanna.Crossref | GoogleScholarGoogle Scholar |
Galiano L, Martínez-Vilalta J, Sabaté S, Lloret F (2012) Determinants of drought effects on crown condition and their relationship with depletion of carbon reserves in a Mediterranean hold oak forest. Tree Physiology 32, 478–489.
| Determinants of drought effects on crown condition and their relationship with depletion of carbon reserves in a Mediterranean hold oak forest.Crossref | GoogleScholarGoogle Scholar | 22499595PubMed |
Gentilli J (1989) Climate of the jarrah forest. In. ‘The jarrah forest: a complex Mediterranean ecosystem’. (Eds B Dell, JJ Havel, N Malajczuk) pp. 23–30. (Kluwer Academic Publishers: Dordrecht, The Netherlands)
Gibson RK, Bradstock RA, Penman TD, Keith DA, Driscoll DA (2014) Changing dominance of key plant species across a Mediterranean climate region: implications for fuel types and future fire regimes. Plant Ecology 215, 83–95.
| Changing dominance of key plant species across a Mediterranean climate region: implications for fuel types and future fire regimes.Crossref | GoogleScholarGoogle Scholar |
Giorgi F, Lionello P (2008) Climate change projections for the Mediterranean region. Global and Planetary Change 63, 90–104.
| Climate change projections for the Mediterranean region.Crossref | GoogleScholarGoogle Scholar |
Grant CD, Koch JM, Bell BT, Londeragan WA (1997) Tree species response to prescribed burns in rehabilitated bauxite mines in Western Australia. Australian Forestry 60, 84–89.
| Tree species response to prescribed burns in rehabilitated bauxite mines in Western Australia.Crossref | GoogleScholarGoogle Scholar |
Hänninen H (2006) Climate warming and the risk of frost damage to boreal forest trees: identification of critical ecophysiological traits. Tree Physiology 26, 889–898.
| Climate warming and the risk of frost damage to boreal forest trees: identification of critical ecophysiological traits.Crossref | GoogleScholarGoogle Scholar | 16585034PubMed |
Havel JJ (1975) ‘Site-vegetation mapping in the northern jarrah forest (Darling Range). I. Definition of site-vegetation types.’ Bulletin 86. (Forests Department Western Australia: Perth)
Hill KD, Johnson LAS (1995) Systematic studies in the eucalypts 7. A revision of the bloodwoods, genus Corymbia (Myrtaceae). Telopea 6, 185–504.
| Systematic studies in the eucalypts 7. A revision of the bloodwoods, genus Corymbia (Myrtaceae).Crossref | GoogleScholarGoogle Scholar |
Huntingford C, Jones PD, Livina VN, Lenton TM, Cox PM (2013) No increase in global temperature variability despite changing regional patterns. Nature 500, 327–330.
| No increase in global temperature variability despite changing regional patterns.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXht1Wiu7bJ&md5=f0c8e4a3f571ceb7471f45e52917a2aaCAS | 23883935PubMed |
Jentsch A, Beierkuhnlein C (2008) Research frontiers in climate change: effects of extreme meteorological events on ecosystems. Comptes Rendus Geoscience 340, 621–628.
| Research frontiers in climate change: effects of extreme meteorological events on ecosystems.Crossref | GoogleScholarGoogle Scholar |
Jönsson AM, Linderson M-L, Stjernquist I, Schlyter P, Bärring L (2004) Climate change and the effect of temperature backlashes causing frost damage in Picea abies. Global and Planetary Change 44, 195–207.
| Climate change and the effect of temperature backlashes causing frost damage in Picea abies.Crossref | GoogleScholarGoogle Scholar |
Kalma JD, Laughlin GP, Caprio JM, Hamer PJC (1992) The occurrence of frost: types, distribution, and prediction. Advances in Bioclimatology 2, 5–12.
| The occurrence of frost: types, distribution, and prediction.Crossref | GoogleScholarGoogle Scholar |
Ladinig U, Hacker J, Neuner G, Wagner J (2013) How endangered is sexual reproduction of high-mountain plants by summer plants? Frost resistance, frequency of frost events and risk assessment. Oecologia 171, 743–760.
| How endangered is sexual reproduction of high-mountain plants by summer plants? Frost resistance, frequency of frost events and risk assessment.Crossref | GoogleScholarGoogle Scholar | 23386042PubMed |
Man R, Kayahara GJ, Dang Q-L, Rice JA (2009) A case of severe frost damage prior to budbreak in young conifers in northeastern Ontario: consequences of climate change? Forestry Chronicle 85, 453–462.
| A case of severe frost damage prior to budbreak in young conifers in northeastern Ontario: consequences of climate change?Crossref | GoogleScholarGoogle Scholar |
Matusick G, Ruthrof KX, Hardy GStJ (2012) Drought and heat triggers sudden and severe dieback in a dominant Mediterranean-type woodland species. Open Journal of Forestry 2, 183–186.
| Drought and heat triggers sudden and severe dieback in a dominant Mediterranean-type woodland species.Crossref | GoogleScholarGoogle Scholar |
Matusick G, Ruthrof KX, Brouwers NC, Dell B, Hardy GStJ (2013) Sudden forest canopy collapse corresponding with extreme drought and heat in a Mediterranean-type eucalypt forest in southwestern Australia. European Journal of Forest Research 132, 497–510.
| Sudden forest canopy collapse corresponding with extreme drought and heat in a Mediterranean-type eucalypt forest in southwestern Australia.Crossref | GoogleScholarGoogle Scholar |
Matusick G, Ruthrof KX, Brouwers NC, Hardy GStJ (2014) Topography influences the distribution of autumn frost damage on trees in a Mediterranean-type Eucalyptus forest. Trees-Structure and Function 28, 1449–1462.
| Topography influences the distribution of autumn frost damage on trees in a Mediterranean-type Eucalyptus forest.Crossref | GoogleScholarGoogle Scholar |
McChesney CJ, Koch JM, Bell DT (1995) Jarrah forest restoration in Western Australia: canopy and topographic effects. Restoration Ecology 3, 105–110.
| Jarrah forest restoration in Western Australia: canopy and topographic effects.Crossref | GoogleScholarGoogle Scholar |
Meiners SJ, Presley GN (2015) Differential damage of late frost to Ozark tree species. The Journal of the Torrey Botanical Society 142, 12–17.
| Differential damage of late frost to Ozark tree species.Crossref | GoogleScholarGoogle Scholar |
Miller-Rushing AJ, Primack RA (2008) Effects of winter temperatures on two birch (Betula) species. Tree Physiology 28, 659–664.
| Effects of winter temperatures on two birch (Betula) species.Crossref | GoogleScholarGoogle Scholar | 18244951PubMed |
Nicault A, Alleaume S, Brewer S, Carrer M, Nola P, Guiot J (2008) Mediterranean drought fluctuation during the last 500 years based on tree-ring data. Climate Dynamics 31, 227–245.
| Mediterranean drought fluctuation during the last 500 years based on tree-ring data.Crossref | GoogleScholarGoogle Scholar |
Orlowsky B, Seneviratne SI (2012) Global changes in extreme events: regional and seasonal dimension. Climatic Change 110, 669–696.
| Global changes in extreme events: regional and seasonal dimension.Crossref | GoogleScholarGoogle Scholar |
Pichler P, Oberhuber W (2007) Radial growth response of coniferous forest trees in an inner Alpine environment to heat-wave in 2003. Forest Ecology and Management 242, 688–699.
| Radial growth response of coniferous forest trees in an inner Alpine environment to heat-wave in 2003.Crossref | GoogleScholarGoogle Scholar |
Poot P, Veneklaas EJ (2013) Species distribution and crown decline are associated with contrasting water relations in four common sympatric eucalypt species in southwestern Australia. Plant and Soil 364, 409–423.
| Species distribution and crown decline are associated with contrasting water relations in four common sympatric eucalypt species in southwestern Australia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXit1Gksb8%3D&md5=36539d6bb2cb1b770861146a88145b5cCAS |
Raut BA, Jakob C, Reeder MJ (2014) Rainfall changes over southwestern Australia and their relationship to the southern annular mode and ENSO. Journal of Climate 27, 5801–5814.
| Rainfall changes over southwestern Australia and their relationship to the southern annular mode and ENSO.Crossref | GoogleScholarGoogle Scholar |
Read J, Hill RS (1988) Comparative responses to temperature of the major canopy species of Tasmanian cool temperate rainforest and their ecological significance. I. Foliar frost resistance. Australian Journal of Botany 36, 131–143.
| Comparative responses to temperature of the major canopy species of Tasmanian cool temperate rainforest and their ecological significance. I. Foliar frost resistance.Crossref | GoogleScholarGoogle Scholar |
Repo T, Hãnninen H, Kellomãki S (1996) The effects of long-term elevation of air temperature and CO2 on the frost hardiness of Scots pine. Plant, Cell & Environment 19, 209–216.
| The effects of long-term elevation of air temperature and CO2 on the frost hardiness of Scots pine.Crossref | GoogleScholarGoogle Scholar |
Ruiz-Labourdette D, Nogués-Bravo D, Ollero HS, Schmitz MF, Pineda FD (2012) Forest composition in Mediterranean mountains is projected to shift along the entire elevational gradient under climate change. Journal of Biogeography 39, 162–176.
| Forest composition in Mediterranean mountains is projected to shift along the entire elevational gradient under climate change.Crossref | GoogleScholarGoogle Scholar |
Ruiz-Labourdette D, Schmitz MF, Pineda FD (2013) Changes in tree species composition in Mediterranean mountains under climate change: indicators for conservation planning. Ecological Indicators 24, 310–323.
| Changes in tree species composition in Mediterranean mountains under climate change: indicators for conservation planning.Crossref | GoogleScholarGoogle Scholar |
Schomaker ME, Zarnoch SJ, Bechtold WA, Latelle DJ, Burkman WG, Cox SM (2007) Crown-condition classification: a guide to data collected and analysis. General technical report SRS-102. United States Department of Agriculture, Forest Service, Southern Research Station, Ashville. NC.
Specht RL, Row ME, Boughton VH (1974) Conservation of major plant communities in Australia and Papua New Guinea. Australian Journal of Botany 1–667.
| Conservation of major plant communities in Australia and Papua New Guinea.Crossref | GoogleScholarGoogle Scholar |
Stanturf JA, Vance ED, Fox TR, Kirst M (2013) Eucalyptus beyond its native range: environmental issues in exotic bioenergy plantations. International Journal of Forestry Research 2013, 463030
| Eucalyptus beyond its native range: environmental issues in exotic bioenergy plantations.Crossref | GoogleScholarGoogle Scholar |
Stone C, Matusuki M, Carnegie A (2003) ‘Pest and disease assessment in young eucalypt plantations: field manual for using the crown damage index.’ (Ed. M Parsons) (National Forest Inventory, Bureau of Rural Sciences: Canberra)
Trenberth KE, Jones PD, Ambenje P, Bojariu R, Easterling D, Klein Tank A, Parker D, Rahimzadeh F, Renwick JA, Rusticucci M, Soden B, Zhai P (2007) Observations: surface and atmospheric climate change In. ‘Climate change 2007: the physical science basis. Contribution of the Working Group I to the fourth assessment report of the Intergovernmental Panel on Climate Change’. (Eds S Solomon, D Qin, M Manning, Z Chen, M Marquis, KB Averyt, M Tignor, HL Miller) (Cambridge University Press: Cambridge, UK)
VanDerWal J, Murphy HT, Kutt AS, Perkins GC, Bateman BL, Perry JJ, Reside AE (2012) Focus on poleward shift in species’ distribution underestimates the fingerprint of climate change Nature Climate Change 3, 239–243.
| Focus on poleward shift in species’ distribution underestimates the fingerprint of climate changeCrossref | GoogleScholarGoogle Scholar |
Vasseur DA, DeLong JP, Gilbert B, Greig HA, Harley CDG, McCann KS, Savage V, Tunney TD, O’Connor MI (2014) Increased temperature variation poses a greater risk to species than climate warming. Proceedings. Biological Sciences 281, 20132612
| Increased temperature variation poses a greater risk to species than climate warming.Crossref | GoogleScholarGoogle Scholar |
Volker PW, Owen JV, Borralho NMG (1994) Genetic variances and covariances for frost tolerance in Eucalyptus globulus and E. nitens. Silvae Genetica 43, 366–372.
Warton DI, Hui FCK (2011) The arcsine is asinine: the analysis of proportions in ecology. Ecology 92, 3–10.
| The arcsine is asinine: the analysis of proportions in ecology.Crossref | GoogleScholarGoogle Scholar | 21560670PubMed |
Williams CM, Henry HAL, Sinclair BJ (2015) Cold truths: how winter drives responses of terrestrial organisms to climate change. Biological Reviews of the Cambridge Philosophical Society 90, 214–235.
| Cold truths: how winter drives responses of terrestrial organisms to climate change.Crossref | GoogleScholarGoogle Scholar | 24720862PubMed |
Woldendorp G, Hill MJ, Doran R, Ball MC (2008) Frost in a future climate: modelling interactive effects of warmer temperatures and rising atmospheric [CO2] on the incidence and severity of frost damage in a temperature evergreen (Eucalptus pauciflora). Global Change Biology 14, 294–308.
| Frost in a future climate: modelling interactive effects of warmer temperatures and rising atmospheric [CO2] on the incidence and severity of frost damage in a temperature evergreen (Eucalptus pauciflora).Crossref | GoogleScholarGoogle Scholar |
Yu L, Zhong S, Bian X, Heilman WE, Andresen JA (2014) Temporal and spatial variability of frost-free seasons in the Great Lakes region of the United States. International Journal of Climatology 34, 3499–3514.
| Temporal and spatial variability of frost-free seasons in the Great Lakes region of the United States.Crossref | GoogleScholarGoogle Scholar |
Zheng B, Chapman SC, Christopher JT, Frederiks TM, Chenu K (2015) Frost trends and their estimated impact on yield in the Australian wheatbelt. Journal of Experimental Botany
| Frost trends and their estimated impact on yield in the Australian wheatbelt.Crossref | GoogleScholarGoogle Scholar | 25922479PubMed |
