Diapositiva 1

Shifting from a fertilization-dominated to a warming- dominated period?

Josep Peñuelas et al.

Global ecology Unit CREAF-CSIC-UAB-UB, Barcelona

Oxford, May 12, 2017 We fertilize the biosphere …with increasing human inputs of CO2 …with increasing human inputs of N

Penuelas et al. Nature Communications 2013 …with warming Advancement of the leaf onset

Leaf onset in the northern hemisphere triggered by daytime temperature Piao et al. Nature Communications, 2015 Delay of the end of season Remote sensing data Northern latitudes

Ground data US, Germany and Switzerland

Jong et al. Nature Communications 2017 ...and with the consequent lengthening of the growth period The global change drivers fertilizing the biosphere

ATMOSPHERIC GASES LAND USE CHANGES

Eutrophication

CLIMATE Biosphere Study Sites with flux towers Site Site name AT-Neu Austria - Neustift/Stubai Valley BR-Ban Brazil - Ecotone Bananal Island BR-Ma2 Brazil - Manaus - ZF2 K34 BR-Sa1 Brazil - Santarem-Km67-Primary Forest CA-Man Canada - BOREAS NSA - Old Black Spruce CA-Oas Canada - Sask.- SSA Old Aspen CA-Obs Canada - Sask.- SSA Old Black Spruce CA-Ojp Canada - Sask.- SSA Old Jack Pine CA-WP1 Canada - Western Peatland- LaBiche DE-Hai Germany - Hainich DE-Meh Germany - Mehrstedt 1 DE-Tha Germany - Anchor Station Tharandt - spruce DE-Wet Germany - Wetzstein ES-LMa Spain - Las Majadas del Tietar FI-Hyy Finland - Hyytiala FR-Pue France - Puechabon HU-Bug Hungary - Bugacpuszta IT-Col Italy - Collelongo- Selva Piana IT-Cpz Italy - Castelporziano IT-Lav Italy - Lavarone (after 3/2002) IT-MBo Italy - Monte Bondone IT-Pia Italy - Island of Pianosa IT-Ro1 Italy - Roccarespampani 1 IT-Ro2 Italy - Roccarespampani 2 IT-SRo Italy - San Rossore NL-Loo Netherlands - Loobos PT-Esp Portugal - Espirra PT-Mi1 Portugal - Mitra (Evora) SE-Nor Sweden - Norunda US-Atq USA - AK - Atqasuk US-Bar USA - NH - Bartlett Experimental Forest US-Ha1 USA - MA - Harvard Forest EMS Tower US-Ho1 USA - ME - Howland Forest (main tower) US-Ho2 USA - ME - Howland Forest (west tower) US-Ivo USA - AK - Ivotuk US-LPH USA - MA - Little Prospect Hill US-Me2 USA - OR - Metolius-intermediate aged ponderosa pine US-Me3 USA - OR - Metolius-second young aged pine US-MMS USA - IN - Morgan Monroe State Forest US-NC2 USA - NC - NC_Loblolly Plantation US-Ne3 USA - NE - Mead - rainfed maize-soybean US-SRM USA - AZ - Santa Rita Mesquite US-Wrc USA - WA - Wind River Crane Site NEP has increased (Eddy covariance data)

Fernandez-Martinez et al Scientific Reports 2017 Increased net ecosystem production with CO2 and N dep

Synthesis data from eddy covariance towers

Fernandez-Martinez et al Scientific Reports 2017 Greening trend a b

c d

Zhu et al. Nature Climate Change, 2016 Greening trend

25-50% greening, 4% browning

Zhu et al. Nature Climate Change, 2016 Greening trend attributed mostly to CO2, and less to warming, Ndep and land cover change

70, 8, 9,4 %

Zhu et al. Nature Climate Change, 2016 Fertilization of the biosphere: Enhancement of NPP and carbon sinks

Land-use Elevated CO Eutrophication Warming 2 changes

(+) NPP and Carbon sink (?) And yet no significant overall tree growth

-1 13C (%o ) iWUE (umol mmol ) Growth (TRW) 18 130 1.2 NS TRW601960s 120 TRW002000s 17 NS *** 1.1 110 16 1 100 15 0.9 90 14 0.8 80

13 70 0.7

12 60 0.6 Penuelas et al GEB 2011 Human population growth offsets climate-driven increase in woody vegetation in sub-Saharan Africa

1992-2011

Brand et al Nature Ecology & Evolution 2017 Enhancement of carbon sinks at slowing pace

The combined land–ocean CO2 sink flux per unit of excess atmospheric CO2 above preindustrial levels has declined over 1959-2012 by a factor of about 1/3 Land use Ratio of residual Fossil fuel change Residual land sink to total emissions emissions land sink emissions

1960-1979 3,88 1,44 1,71 0,32

1986-2015 8,42 1,50 2,10 0,21

Penuelas et al submitted to Nature Ecology & Evolution 2017 Attribution of Recent Acceleration of Atmospheric CO2 1970 – 1979: 1.3 ppm y-1 1980 – 1989: 1.6 ppm y1 To: 1990 – 1999: 1.5 ppm y-1 • Economic growth -1 • Carbon intensity 2000 - 2010: 1.9 ppm y • Efficiency of natural sinks

65% - Increased activity of the global economy

17% - Deterioration of the carbon intensity of the global economy

18% - Decreased efficiency of natural sinks

Canadell et al. 2007, PNAS, Peters et al Nature 2011 Fertilization of the biosphere: Enhancement of NPP and carbon sinks

Land-use Elevated CO Eutrophication Warming 2 changes

(+) NPP and Carbon sink (?) Likely limitations for enhancement of carbon sinks

Land-use Elevated CO Eutrophication Warming 2 changes (+) (+) (+) (-) Air pollution Drought Nutrient Afforestation (-) N (-) limitations (-) Reforestation P (-) (-) (+) (-)

(+) (?) (+) (?) (+) (?) (?) (-)

(+) Carbon sink (?)

Data: Eddy covariance Forest Tree rings Annual rate of Satellite inventories CO2 increase Revisiting nutrients and net ecosystem production

Global data set for forest sites

)

-1 Nutrient-rich: Slope = 0.73, P = 0.002 0,4 1600 Nutrient-poor: Slope = 0.09, P = 0.01 0,3 year Nutrient-poor (GPP < 2500): Slope = 0.35, P < 0.001

-2 Nutrients * GPP P < 0.0001 0,2

1200 CUEe *** 0,1 800

400

-400

Net Ecosystem Productionm (gC Ecosystem Net

0 500 1000 1500 2000 2500 3000 3500 4000 Gross Primary Production (gC m-2 year-1) Fernández-Martínez et al. Nature Climate Change 2014 Nutrients and ecosystem respiration Global data set for forest sites 4000 Nutrient-rich: Slope = 0.25, P = 0.14

) -1 3500 Nutrient-poor: Slope = 0.90, P < 0.0001 Nutrient-poor (GPP < 2500): Slope = 0.64, P < 0.0001

year Nutrients * GPP P < 0.0001 -2 3000

2500

2000

1500

1000

500

Ecosystem Respiration (gC m Respiration (gC Ecosystem 0 0 500 1000 1500 2000 2500 3000 3500 4000

Gross Primary Production (gC m-2 year-1) Fernández-Martínez et al. Nature Climate Change 2014 Nutrient impacts on net ecosystem production

Nature Climate Change 2014 Revisiting nutrient fertilization The phosphorus imbalance in Nature

Phosphorus supply Phosphorus demand to natural ecosystems is growing due to is limited human activities

• Ash and dust deposition • Increasing CO2, global • Free-up inaccessible soil P effect • Weathering of mineral P • Increasing N deposition, mainly over industrialized All small & uncertain processes regions • Climate change, e.g. longer growing seasons in boreal areas The phosphorus imbalance in Nature

Phosphorus supply Phosphorus demand to natural ecosystems is growing due to is limited human activities

The P-imbalance will alter ecosystems, carbon sinks, and climate Natural ecosystems response

Molecular. Genetics, metabolomics, chemical ecology. Individual. Growth. Population. Adaptation, extinction. Community. Species interactions, species composition. Ecosystem. Productivity, biogeochemistry, gas fluxes

Regional and global variation in these processes Natural ecosystems response

Imbalance-P Experiments Arctic zone (Greenland) Subarctic zone (Iceland) Boreal zone (Sweden) Wet temperate zone (Belgium, China) Mediterranean zone (Spain) Desert (Mexico) Tropics (French Guiana, Ecuador, Brazil, Hawaii, Borneo) The phosphorus imbalance in tropical areas

• During the 21st century: • N deposition will continue, but slow down, over northern areas. • N deposition will increase specially over tropical areas.

1990 2050

• This will cause the N to P deposition ratio to increase. • Unlike northern ecosystems, most tropical forests are more limited by P than by N. The phosphorus imbalance in tropical areas

• During the 21st century: • N deposition will continue, but slow down, over northern areas. • N deposition will increase dramatically over tropical areas.

Knowledge gap for the phosphorus imbalance of tropical forests and its consequences

• This will cause the N to P deposition ratio to increase. • Unlike northern ecosystems, most tropical forests are more limited by P than by N. Special focus on tropics and French Guiana

Knowledge gap in tropical forests

Guiana is representative for tropics • 50% of global soil types • very large precipitation gradient

Active research already field sites, historical data, staff

…also Ecuador, Brazil, Borneo, Hawaii French Guiana transect Guyafor

Grau et al. Scientific Reports, 2017 Topographic profile Fertilization experiments N,P, NP Factors driving the nutrient supply

Emissions and deposition of P

Table 2. Global budget of Phosphorus in the atmosphere. All uncertainties are given as 90% confidence intervals in brackets.

Fluxes, Tg P yr-1

Sources

Combustion (present study) a 1.8 (0.5 to 4.4)

Anthropogenic 1.1 (0.3 to 3.1)

Natural 0.7 (0.2 to 1.3)

Mineral dust input b 0.8 (0.2 to 1.8)

Biogenic aerosol particles c 0.58 (0.16 to 1.0)

Volcanoes d 0.006±0.003

Sea salt e 0.16 (0.0049 to 0.33)

Total sources 3.4 (2.0 to 6.3)

Sink

Deposition over land f 3.2±1.7 (estimate for 1954–2012)

Deposition over oceans g 0.45 (0.15 to 1.35) (estimate for 1960–1976)

Total sinks 3.7 (2.8 to 5.0)

Wang et al Nature Geoscience 2015 d

° Factors driving N

the P supply 30

0 Pre-industrial

Pre-industrial 60

° (1850)

S ° Present

Present 60

(1997-2013) S

P deposition 60

30 2100

Future 60

° (2100 RCP8.5)

P deposition rate (mg m-2 yr-1) 0.1 0.5 1 2 Wang4 10 2 0et 4 0al 8Nature0 160 Geoscience 2017 Impacts on ocean’s NPP

60 2 4.4 8.2 slope = – 15.2 ± 1.8, r =0.55 slope = – 0.35 ± 0.10, r2=0.18 slope = – 0.83 ± 0.23, r2=0.18

2 A B 2 C 2

)

) slope = – 13.3 ± 1.6, r =0.53 ) slope = – 0.21 ± 0.10, r =0.08 slope = – 0.74 ± 0.22, r =0.16

- - 7.8 4.2 55 Warming 7.4 4.0 + AAD 7.0 50 Warming 3.8

NPP (Pg C yr (Pg NPP

NPP (Pg C yr (Pg NPP alone C yr (Pg NPP 6.6 All stratified oceans North Atlantic South Atlantic 45 3.6 6.2 19.5 19.7 19.9 20.1 17.4 17.6 17.8 18.0 17.4 17.6 17.8 18.0 SST (°C) SST (°C) SST (°C)

11 2 23 15 slope = – 2.56 ± 0.46, r =0.35 slope = – 7.00 ± 0.93, r2=0.49 slope = – 1.10 ± 0.33, r2=0.54

D E 2 F 2

)

) slope = – 1.96 ± 0.40, r =0.30 ) slope = – 6.67 ± 0.91, r =0.48 slope = – 0.83 ± 0.33, r =0.52

- 10 - 21 14

9 19 13

8 17 12

NPP (Pg C yr (Pg NPP

NPP (Pg C yr (Pg NPP North Pacific South Pacific Indian Ocean 7 15 11 20.6 20.8 21.0 21.2 21.4 20.6 20.8 21.0 21.2 21.4 19.2 19.4 19.6 19.8 20.0 SST (°C) SST (°C) SST (°C) increasing anthropogenic aerosol deposition (AAD) Relationship between net primary production (NPP) and annual mean sea-surface temperature (SST) for 1948-2007 Wang et al 2015 Geophysical Research Letters Factors driving the P supply: Phosphatases

Proportional enzyme activity ratios

TROPICAL P limitation

enzyme MEDITERRANEAN

N limitation

/ (C+ N) N) (C+ /

enzyme C C C enzyme / (C+ P) enzyme Stoichiometry and global C cycle: N and P demand in Earth System Models Simulated coupled (top panel) and uncoupled (lower panel) response of terrestrial carbon fluxes and stocks from the C4MIP and CMIP5 climate carbon cycle model ensemble. The NPP-P requirement is estimated based on the stoichiometric ratios of Kattge et al. (GCB 2011), assuming that woody NPP is 1/3rd of total NPP and active tissues (leaves/roots) are 2/3rds

Penuelas et al 2013 Nature Communications 2013 D

i Fig. 2. The simulated P in vegetation (top left), sorbed P (top right), P in soil organic matter and s

litter (bottom left), and the annual P uptake by vegetation (bottom right) for present day. s

3227 |

e Reduced Terrestrial Carbon Sinks? Nutrient limitation? r

Our preliminary data suggest an overlooked global P D

limitation of carbon sequestration during the 21st century. c

C4MIP and CMIP5 models s

n C)

P Pg

400 a

r 200

Less biomass | 0 if P limitation

D Biomass increase Biomass ( increase

1900 2100 2300 2500 i

Year c

N limitation o uncertainty range n

P limitation a threshold p

-Penuelas et al. Nature Comm. 2013 r -Goll et al. Biogeociences 2013

Fig. 3. The simulated change in land carbon storage under the SRES A1B scenario. Shown are s

i the 10 yr mean of soil temperature (a), the CO2 concentration as used in the forcing simulation o

(b), the resulting change in total land C storage (c), and the changes in the two main land P

compartments vegetation (d) and soil (e). p

3228 | Diagnosing phosphorus limitations in carbon cycle models

Sun et al GCB 2016

Nutrients may limit current and future NPP

N N limits

CMIP5 CMIP5 Mean N+P limits Year New inputs of N and P are probably insufficient to meet the nutrient demand generated from projected productivity increases, and highlights the potential for nutrient limitation to ultimately constraint NPP, especially in tropical ecosystems. Wieder et al. (2015) Nature Geoscience Likely limitations for enhancement of carbon sinks

Land-use Elevated CO Eutrophication Warming 2 changes (+) (+) (+) (-) Air pollution Drought Nutrient Afforestation (-) N (-) limitations (-) Reforestation P (-) (-) (+) (-)

(+) (?) (+) (?) (+) (?) (?) (-)

(+) Carbon sink (?)

Data: Eddy covariance Forest Tree rings Annual rate of Satellite inventories CO2 increase Heat waves

Observed changes in FAPAR from the MODIS–Terra–EOS satellite.

-0.4 +0.4

2003 (strong anomalous net source of carbon dioxide 0.5 Pg C y-1) Ciais et al Nature 2005 Revisiting phenological effects of warming

Decreasing temperature sensitivity 40%

Declining global warming effects on the phenology of spring leaf unfolding

Fu et al. Nature 2015 Positive Sensitivity of NDVI growth to rising Tmax (a) but negative to rising Tmin (b)

Peng et al. Nature 2013 Positive Sensitivity of NCE to rising Tmax but negative to rising Tmin at northern latitudes

3 T T max min

)

-1 2 * 1

-1

Sensitivity of NCE Sensitivityto of -2

temperature (Pg C °C C(Pg temperature ** -3 Boreal Temperate Peng et al. Nature 2013 Positive Sensitivity of AMP to rising Tmax but negative to rising Tmin at northern latitudes

60 T T max min

) 40 **

-1 20

-20

Sensitivity of AMP to AMP Sensitivityof temperature (% °C (% temperature -40 ** -60 Barrow Mauna Loa Peng et al. Nature 2013 Warming impacts on C uptake and storage …… Frozen carbon, 1600 Pg C Boreal forests 50 Pg C

Tropical forest 400 Pg C Temperate forest 41 Pg C Revisiting drought and growth period

GROWING SEASON

DRY YEAR

Growth

- GPP

JANUARY DECEMBER Responses of organisms and ecosystems to climate change

Molecular. Genetics, metabolomics, chemical ecology. Individual. Growth. Population. Adaptation Community. Species interactions, species composition. Ecosystem. Productivity, biogeochemistry, gas fluxes

Regional and global variation in these processes

Penuelas et al Global Change Biology 2013 • French Guiana: Paracou and Nouragues stations

Tropical Forest, French Guiana (NE South America) Experimental analyses of impacts of climate change

Mediterranean shrubland site: Garraf Natural Park, Catalonia. Population genomic changes: Experimental evidence for selection response

0.5 A) Drought vs. control 0.4

0.3 All individuals established during the duration 258L90 151L05 0.2 of the experiment genotyped at 337 AFLP loci 153L07 158L10 259L91 0.1 N = 40 drought; 29 warming; 45 control 0.0

) -0.1-0.10.5 st B) Warming vs. control

( 0.4

0.3 Drought vs. control: AGTC476 153L07 0.2 158L10

Five outlying loci, P = 0.001 to <0.00001 0.1 259L91 258L90 151L05 0.0

-0.1-0.10.5 Warming vs. control: Genetic differentiation C) Drought vs. warming 0.4

Two outlying loci, P = 0.0030 0.3

0.2 AGTC476 Common outliers involved in both 0.1 151L05 259L91 258L90 0.0 comparisons – implicating drought as the 153L07 158L10 -0.1 selection pressure 0.0 0.1 0.2 0.3 0.4 0.5 0.6 Heterozygosity

Jump et al. 2008 Global Change Biology 14, 637–643.

Jump et al. 2008, Global Change Biology, Changes in Methylation of DNA (epigenetic changes) in droughted Quercus ilex

Prades forest (Catalonia): experimental field site

Rico et al Plant Biology 2014, Barbeta et al Global Change Biology 2013 Changes in stoichiometry and metabolomics: Leaves

Drought:

· Antioxidant production (Quinic acid, Tartaric acid)

· K accumulation

· Choline and osmolites accumulation (especially in Summer) 1.0 Roots 32

19 Warming: 18 30

0.5 Compounds11 related 20 toKthe Amino acid and sugar9 31 · Fatty acids increases N:P 23 57 metabolism 59 DROUGHT61 64 52 58 55 62 21 51 50 53 13 724954 60 N:P 69 3 Secondary7147 metabolites 14 28 38 274126 45 48 1224 685644 37 25 0.0 (terpene and phenolics70 ) 4 6 · RCASS increases 5 29 and Fatty acids 46 10 63 Sugars 34 43 22 8 39 65 40 66 1 35 7 · P decreases 67 Amino acids 16 DROUGHT 2 17 33 -0.5 36 15

Metabolome PC3 (8%)

-1.0 -1.0 -0.5 0.0 0.5 1.0 Rivas-Ubach et al PNAS 2013 Metabolome PC1 (37%) Gargallo et al New Phytologist 2015 ESTUDIOS EXPERIMENTALES: PREDICCIONES Experiments in Garraf Changes in growth

Penuelas et al Global Change Biology 2007 Demography: seedling establishment

Lloret et al Global Change Biology 2004 Community changes

The responses of 4 representative species

Liu et al, New Phytologist 2017 VULCAN Mediterranean shrubland

Production and biomass changes Liu et al, New Phytologist 2017 Defoliation Crown defoliation responses: Species-specific trends in Spanish forests

Drought induced defoliation in 16 dominant tree species Carnicer et al. PNAS 2011 Defoliation Crown defoliation responses: Mediterranean and European trends

Carnicer et al. PNAS 2011 Decreased tree growth in the Mediterrranean region Ongoing drought periods in the Eastern and Western Mediterranean basin are the most severe since the 16th and 17th centuries

(Guiot et al 2005, Luterbacher et al 2009, Nicault et al. 2008, Barriendos and Rodrigo 2005) Drought Effects on the Mid-Latitude Carbon Sinks

A number of major droughts in mid-latitudes have contributed to the weakening of the growth rate of terrestrial carbon sinks in these regions.

NDVI Anomaly 1982-2004 Summer 1982-1991 [Normalized Difference Vegetation Index]

Summer 1994-2002/04

Angert et al. 2005, PNAS; Buermann et al. 2007, PNAS; Ciais et al. 2005, Science Science 2010 Likely limitations for enhancement of carbon sinks

Land-use Elevated CO Eutrophication Warming 2 changes (+) (+) (+) (-) Air pollution Drought Nutrient Afforestation (-) N (-) limitations (-) Reforestation P (-) (-) (+) (-)

(+) (?) (+) (?) (+) (?) (?) (-)

(+) Carbon sink (?)

Data: Eddy covariance Forest Tree rings Annual rate of Satellite inventories CO2 increase Simple conceptual framework for carbon sink trends

퐶푎푟푏표푛 푠푖푛푘 푡푟푒푛푑 ∶ 퐶푠 = 푁푃푃 − 푘 퐶 − 푘 퐶

-The forcing: 푁푃푃 = 푛푒푡 푝푟푖푚푎푟푦 푝푟표푑푢푐푡푖푣푖푡푦

1 -푘C, with 푘 = 푡푢푟푛표푣푒푟 푟푎푡푒 표푓 푒푥푐푒푠푠 푐푎푟푏표푛 푖푛 푒푐표푠푦푠푡푒푚 퐶 푝표표푙푠 = , and 퐶 = 휏 풄풂풓풃풐풏 풔풕풐풄풌, is the modulation of the sink trend by turnover rates changes, i.e. increase of k due to priming, increased mortality, replacement of high biomass forests by lower biomass ones.

-The third term is the equilibrium elasticity, i.e. given a C sink at time t, the carbon cycle wants to restore equilibrium at time t’ > t and makes this sink decrease in case of no change of NPP and k (i.e. first and second terms zero). 퐶푎푟푏표푛 푠푖푛푘 ∶ 퐶 = 푁푃푃 − 푘퐶

Impacts on net ecosystem production: Sensitivities to CO2 and T

Penuelas et al submitted to Nature Ecology and Evolution 2017 Earth System & Climate response Land-use Elevated CO Eutrophication Warming 2 changes (+) (+) (+) (-) Air pollution Drought Nutrient Afforestation (-) N (-) limitations (-) Reforestation P (-) (-) (+) (-)

Shifting to (+)a warming (?) period(+) with(?) more(+) frequent (?) extreme(?) conditions(-) that surpass thresholds and tipping points

(+) Carbon sink (?)

Data: Eddy covariance Forest Tree rings Annual rate of Satellite inventories CO2 increase

Penuelas et al submitted to Nature Ecology and Evolution 2017 Obervations: Regional abrupt shifts: Iberian peninsula Impacts: abrupt decreases in carbon storage Holocene Mediterranean regions

Trees versus Forest Shrubs Versus Scrubland:

Eg. Holocene changes in study site in Almeria, Spain Assessment of radiation use efficiency and carbon uptake EVERYWHERE ALL THE TIME: Remote sensing 2- Biochemical, optical and odorous signals of the energetic and nutrient status of plants and ecosystems

Penuelas et al Trends in Plant Science 2015 Remote sensing of radiation use efficiency: the PRI

PAR

Chl* Electron Transport carboxilation

Fluorescence Heat Heat dissipation is linked to the production of Zeaxanthin Zeaxanthin is linked to the leaf reflectance at 531 nm PRI= (R531-R570)/(R531+R570)

Photochemical reflectance index

Gamon, Peñuelas, Field RSE 1992 Peñuelas , Filella, Gamon NP 1995 Leaf level measurements Development of methods Biochemical, optical and odorous signals of the energetic status of plants and ecosystems

Zhang et al Remote Sensing 2016 Study Sites Site Site name AT-Neu Austria - Neustift/Stubai Valley BR-Ban Brazil - Ecotone Bananal Island BR-Ma2 Brazil - Manaus - ZF2 K34 BR-Sa1 Brazil - Santarem-Km67-Primary Forest CA-Man Canada - BOREAS NSA - Old Black Spruce CA-Oas Canada - Sask.- SSA Old Aspen CA-Obs Canada - Sask.- SSA Old Black Spruce CA-Ojp Canada - Sask.- SSA Old Jack Pine CA-WP1 Canada - Western Peatland- LaBiche DE-Hai Germany - Hainich DE-Meh Germany - Mehrstedt 1 DE-Tha Germany - Anchor Station Tharandt - spruce DE-Wet Germany - Wetzstein ES-LMa Spain - Las Majadas del Tietar FI-Hyy Finland - Hyytiala FR-Pue France - Puechabon HU-Bug Hungary - Bugacpuszta IT-Col Italy - Collelongo- Selva Piana IT-Cpz Italy - Castelporziano IT-Lav Italy - Lavarone (after 3/2002) IT-MBo Italy - Monte Bondone IT-Pia Italy - Island of Pianosa IT-Ro1 Italy - Roccarespampani 1 IT-Ro2 Italy - Roccarespampani 2 IT-SRo Italy - San Rossore NL-Loo Netherlands - Loobos PT-Esp Portugal - Espirra PT-Mi1 Portugal - Mitra (Evora) SE-Nor Sweden - Norunda US-Atq USA - AK - Atqasuk US-Bar USA - NH - Bartlett Experimental Forest US-Ha1 USA - MA - Harvard Forest EMS Tower US-Ho1 USA - ME - Howland Forest (main tower) US-Ho2 USA - ME - Howland Forest (west tower) US-Ivo USA - AK - Ivotuk US-LPH USA - MA - Little Prospect Hill US-Me2 USA - OR - Metolius-intermediate aged ponderosa pine US-Me3 USA - OR - Metolius-second young aged pine US-MMS USA - IN - Morgan Monroe State Forest US-NC2 USA - NC - NC_Loblolly Plantation US-Ne3 USA - NE - Mead - rainfed maize-soybean US-SRM USA - AZ - Santa Rita Mesquite US-Wrc USA - WA - Wind River Crane Site Example of ecosystem scale in a Mediterranean forest Gamon et al. PNAS 2016 Development of methods Biochemical, optical and odorous signals of the energetic status of plants and ecosystems

Gamon et al PNAS 2016

CCI vs. GEP – All Sites Daily GEP Daily

CCI [PRI(11,1)] Global observations of plant fluorescence

Frankenberg et al Joiner et al Guanter et al CO2 uptake Assessment EVERYWHERE ALL THE TIME PRI + NDVI

Dissipation of excess radiation Leaves, Canopies, Zeaxanthin and other carotenoids Ecosystems Morphological and physiological changes

0.5 0.4

0.3

0.2 Decreased reflectance at 531 nm Reflectance 531 nm 0.1 0 400 500 600 700 800 900 1 10 3 Wavelength (nm) PRI = R531- R570/R531+ R570 Light use efficiency

NDVI, EVI,… APAR

Gross primary productivity 2- Biochemical, optical and odorous signals of the energetic and nutrient status of plants and ecosystems

Penuelas et al Trends in Plant Science 2015 Biological functions of BVOCs Biochemical security valves Protection, defense, reproduction, communication,…

Plant protection against stress Thermotolerance Oxidative stress tolerance Photoprotection Plant reproduction Pollination Fruit and Seed dispersal Plant defense

Indirect defense against herbivores Direct defense against pathogens Plant-plant interaction Direct defense against Communication herbivores Allelopathy

Penuelas et al Trends Plant Science 2010 EFFECTS OF CLIMATE AND ATMOSPHERIC CHEMISTRY ON BVOCS IN A COMPLEX NETWORK OF INTERACTIONS Effects of increased BVOCs on atmospheric chemistry and climate

Climate Warming + NO 2 O3 + - NO + OH CH4 lifetime Release of latent NO3 heat of water O3 condensation

Aerosols and CCN + VOCs + CO2

Increased biogenic volatile organic compounds

Penuelas et al Trends Plant Science 2010 Formation of aerosol particles from highly oxygenated molecules produced by ozonolysis of a-pinene

Kirkby et al Nature 2016 Eutrophication Drought Warming Elevated CO2

(+) (-)

(-)

(-) Oxidative stress (-?) and less carbon gain (+) (-)

Direct Tropospheric Secondary Ozone effects Organic Aerosol (+) (+-) (+) (-+) (+) (+) (+) (+) (+) (+) (+-) Constitutive Induced Leaf level (+) Indirect BVOC emission BVOC emission effects Species distribution standing biomass Stand level

Land use (+) changes Changed (increased) BVOC fluxes Penuelas & Staudt Trends in Plant Science 2010 Foliar and branch chambers, eddy covariance, Inverse modelling based on atmospheric concentrations, modelling…but to reach “EVERYWHERE (MOST PLACES) ALL (MOST OF) THE TIME”: remote sensing

Remote sensing of BVOCs Remote sensing of formaldehyde

Guenther et al. 2006

Indirect approaches through the detection of one of its oxidation products: formaldehyde. This approach relies on assumptions associated with the oxidant chemistry relating isoprenoids to formaldehyde that are subject to significant uncertainties. Processes underlying isoprene emissions linked to processes underlying CO2 uptake (they could thus be assessed with PRI)

Morfopoulos et al New Phytologist PAR Excess of reducing power: Isoprenoid synthesis NADPH and ETR Chl* Electron Transport carboxilation LUE

Fluorescence Heat dissipation linked to the production of Zeaxanthin (531 nm) PRI= (R531-R570)/(R531+R570) Photochemical reflectance index

Will PRI also estimate isoprenoid emissions? +LUE -LUE Leaf level measurements Isoprenoid emissions inversely related to LUE

Populus nigra

Control Isoprene

Senescence

Drought

Quercus ilex Monoterpenes Control

Drought

LUE Penuelas et al Nature Comm 2013 Isoprenoid emissions inversely related to PRI

Populus nigra

Control

Isoprene Senescence

Drought

Quercus ilex

Control Monoterpenes

Drought

PRI Penuelas et al Nature Comm 2013 Isoprenoid emissions inversely related to LUE and PRI

All conditions together

Isoprene

Monoterpenes

Penuelas et al Nature Comm 2013 Modelling with Emission factors, PAR, T, seasonality,…… to reach a potential emission rate at particular conditions. PRI helps to provide the actual rate.

Adding PRI to the MEGAN model estimation of isoprenoid emissions Measured

Estimated

Penuelas et al Nature Comm 2013 PRI 0.25 = 0.60 = 2 R 0.2 ) 0.15 Filella et al. 2017 Filella PRI 0.1 0.05 0

5 0

25 20 15 10

) h m (mg emission Isoprene

-1 -2 0.25

of the Missouri Ozarks (central USA) (MOFLUX USA) (central of Missouri the Ozarks

efficiency Photosynthetic forest 0.2 0.15 temperate PRI 0.1 deciduous = 0.643= 2 0.05 R Broadleaf 0 0 0.01

0.002 0.006 0.004 0.008 0.014 0.012

2 -0.002

LUE (mol CO (mol LUE mol photons mol ) -1 Upscaling campaigns

In sites with different MOT plant biomass-land cover MOG GAR

1,0 1,0 PRA 0,9 0,9

0,8 0,8

0,7 0,7

0,6 0,6

EVI 0,5 0,5

NDVI NDVI 0,4 0,4

MOG GAR 0,3 0,3

0,2 0,2

0,1 0,1

3,0 1,0

April 2,5 July 0,8

2,0

0,6 FPAR PRA MOT April 1,5 July

LAI 0,4 1,0

0,2 CREAF 0,5 NCAR 0,0 0,0 IBIMET-CNR Monegros Garraf Prades Montseny Monegros Garraf Prades Montseny Sites Gas, water, BVOCs and energy Bottom-up approach balances in different land covers

Satellite Vertical profiles Aircraft

Masts

Tethered balloons

Flux tower

Leaf chamber Aircraft Second balloon (up to 400m) VOC flux

First balloon (up to 100m)

Footprint

Plant emissions (sp, cover) Heterogeneity Vertical slice:

Horizontal Slice: Horizontal slice:

λ / z ≈ 9

(%) i Q

Duration ≈ 1.5 hrs x (km) Isoprene and monoterpene exchange

MOG GAR April July 1.8

)

-1 Monegros (Thymalea tinctoria)

h Garraf (Quercus coccifera)

-2 Prades (Quercus ilex) Montseny (Fagus sylvatica) 1.2

PRA MOT

0.6

Isoprene emission (mgm rate

)

-1

-2 4.0

3.0

2.0

1.0

Monoterpene emissionrate(mgm 0 0 24 0 24 48 Time (hours) 2 Km diameter

Penuelas et al Atmospheric Environment 2013 Satellite Relationships of isoprenoid emissions with PRI at the ecosystem level?

3 y = 1.68- 140.63x R2= 0.89 2.5

1.5

0.5

Isoprene+Monoterpenes (ppbv) Isoprene+Monoterpenes 0 -0.01 -0.005 0 0.005 0.01 PRI 5000m MODIS PRI

Kefauver et al IGARSS 2015, Zhang et al . 2017 Relationships of isoprenoid emissions with PRI at the regional and global level? CO2 uptake Assessment EVERYWHERE ALL THE TIME PRI + NDVI

Dissipation of excess radiation Leaves, Canopies, Zeaxanthin and other carotenoids Ecosystems Morphological and physiological changes

0.5 0.4

0.3

0.2 Decreased reflectance at 531 nm Reflectance 531 nm 0.1 Potential Emission factors 0 400 500 600 700 800 900 1 10 3 MEGAN model Wavelength (nm) PRI = R531- R570/R531+ R570 Light use efficiency

NDVI, EVI,… APAR

Gross primary productivity Isoprenoid emissions This research is timely and important to these five planetary risks

The World Economic Forum identifies among the top risk items for the future :

• Rising greenhouse gas emissions • Failure of climate adaptation • Food shortage crises • Income disparity • Mineral resource supply vulnerability Earth System and climateSocietal consequences responses

Breakthrough : integration with earth system model

Accounting for Realism and climate and feasibility of policy nutrient feedbacks goals Food shortage

Zhao et al. Nature Plants, 2017 Technological Solutions for scenarios storylines Earth System and climateSocietal consequences responses

Technological improvements

Complicated efficiency Potentially transformational enhancing technologies technologies

Integrated nutrient management Algae farm to produce animal feed and recycle through composting P in a nearly closed loop Integrated assessment models Total annual primary energy production

Walsh et al Carbon Balance and Management 2015, Nature Climate Change 2016 Integrated assessment models

Walsh et al Nature Communications 2017 Integrated assessment models

Walsh et al Nature Communications 2017 1-Reduced increase in carbon sink rates: from a fertilization to a warming period

Land use Elevated CO Eutrophication Warming 2 changes (+) (+) (+) (-) Air pollution Drought Nutrient (-) N (-) Aforestation limitations (-) Reforestation P (-) (-) (+) (-) Fires Harvest

NPP: (+) (?) (+) (?) (+) (?) (?) (-)

C residence times (-) (?) (+) (?) (-) (?) (-) (?)

(+) Carbon sink (?)

Data: Eddy covariance Forest Tree rings Annual rate of

Satellite inventaries CO2 increase 2- Biochemical, optical and odorous signals of the energetic and nutrient status of plants and ecosystems 3- Earth System Models and Integrated Assessment Models • Iolanda Filella • Marc Estiarte • Joan Llusià • Romà Ogaya • Jordi Sardans • Alistair Jump Thanks! • Patrícia Prieto • Francisco Lloret • Laura Llorens • Sue Owen • Loles Asensio • Angela Ribas • Jenny Hunt • Martín Garbulsky • Roger Seco • Salvador Blanch • Jorge Curiel, • This Rutishauser, • Alfredo DiFilippo… • Monica Mejia, • Jofre Carnicer • Adrià Barbeta • Ander Anchoategui • Gerard Farre • Shawn Kefauer • Albert Rivas • Albert Gargallo • Albert Porcar • Aleixandre Verger • Mireia Bartrons • Daijun Liu • Chao Zhang • Lei Liu • Marcos Fernández-Martinez • Oriol Grau • Guille Peguero • Pere Roc Fernandez • Anna Escolà • Marta Ayala • Rosa Casanova • Beni stocker • Ivan Janssens • Philippe Ciais Michael Obersteiner