Glacial Amazonia at the canopy-scale: Using a biophysical model to understand forest robustness

Quaternary Science Reviews 171 (2017) 38e47

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Glacial Amazonia at the canopy-scale: Using a biophysical model to understand forest robustness Hiromitsu Sato*, Sharon Anne Cowling Department of Earth Sciences, University of Toronto, Canada

a r t i c l e i n f o

a b s t r a c t

Article history: Received 22 September 2016 Received in revised form 24 April 2017 Accepted 26 June 2017

A canopy-scale model (CANOAK) was used to simulate lowland Amazonia during the Last Glacial Maximum. Modeled values of Net Ecosystem Exchange driven by glacial environmental conditions were roughly half the magnitude of modern fluxes. Factorial experiments reveal lowered [CO2] to be the primary cause of reduced carbon fluxes while lowered air temperatures enhance net carbon uptake. LGM temperatures are suggested to be closer to optimal for carbon uptake than modern temperatures, explained through the canopy energy balance. Further analysis of the canopy energy balance and resultant leaf temperature regime provide viable mechanisms to explain enhanced carbon-water relations at lowered temperatures and forest robustness over glaciations. An ecophysiological phenomena known as the ‘cross-over’ point, wherein leaf temperatures sink below air temperature, was reproduced and found to demarcate critical changes in energy balance partitioning. © 2017 Elsevier Ltd. All rights reserved.

Keywords: Palaeoecology Palaeoclimatology Amazon Biodiversity Canopy model Ecophysiology Last glacial maximum Carbon balance Forest resilience

1. Introduction A sizable body of palynological and palaeovegetative modeling studies provide a justifiable estimate of lowland Amazonian palaeoecology over glacial-interglacial cycles. Pollen records have determined Pleistocene floristic composition and corresponding palaeoclimates, providing grounds to reconstruct past biome distributions and characteristics (Bush et al., 2004) (Burbridge et al., 2004) (Haberle and Maslin, 1999) (Mayle et al., 2000) (Oliveira, 1992). Unfortunately, complete pollen records in the Amazonian lowlands that date back to the Last Glacial Maximum (LGM) are scarce and large-scale inferences must be made from a limited data set (Mayle et al., 2009). To compliment these empirical efforts, modelers have applied several process-based, regional scale models to answer similar questions while searching for underlying ecological mechanisms and feedbacks (Marchant et al., 2004) (Marchant et al., 2006) (Beerling and Mayle, 2006) (Cowling et al., 2001). Synthesis of these two independent approaches has been fruitful but we are still far from a complete understanding of past

* Corresponding author. E-mail address: [email protected] (H. Sato). http://dx.doi.org/10.1016/j.quascirev.2017.06.027 0277-3791/© 2017 Elsevier Ltd. All rights reserved.

climatic changes and ecological responses in Amazonia. The current consensus is that Amazonian forests retained a closed-canopy over glaciations, refuting Haffer's Refugia Hypothesis that proposed dramatic biome fragmentation and the formation of savanna-enclosed patches of moist forest (Haffer, 1969). This theory is consistent with both pollen records from lowland evergreen forest and the Amazon fan, as well as regional modeling studies (Bush and Oliveira, 2006) (Colinvaux et al., 2000) (Cowling et al., 2001) (Marchant et al., 2004). The simulated maintenance of forest cover was proposed to originate in improved carbon-water relations correlated with cooler air temperatures, allowing continued dominance of forests against encroaching grasslands. There is, however, evidence of expanded savannah in marginal regions of Amazonia despite general forest robustness, suggesting limits to the effects of enhanced carbon-water relations (Burbridge et al., 2004) (Mayle et al., 2000). The carbon storage of glacial forests has also been suggested to have been significantly lower (
50%) than that of pre-Industrial Amazonia (Beerling and Mayle, 2006). Cowling also found glacial forest canopy density to be lower and more heterogeneous than that of modern lowland forests, attributing these differences to low atmospheric carbon dioxide rather than temperature or aridity. Conversely, at more extreme values, lower air temperature can also diminish forest cover as

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deduced by studies on Andean sites of much higher elevation (Mourguiart and Ledru, 2003). A motivation for our study is to develop a more comprehensive and quantitative foundation behind these processes. After determining what happened to Amazonian forests during climatic change, it is our intention to address how and why it happened. To do this, we investigate the specific ecological processes that can account for the larger scale changes that comprise our current picture of Pleistocene Amazonia over glacialinterglacial cycles. Our tool of choice is a canopy-scale model (CANOAK), built to capture and quantify finer scale phenomena outside the scope of previous studies. This approach puts a greater emphasis on ecophysiology, the study of an ecosystem and its components’ physiological interactions with the environment, which connects closely with modern forestry and carbon modeling. With this method, we can also explore the broader implications of these ecosystem processes, connecting to topics such as biome stability, drivers of biodiversity, and the projection into the future of Amazonia.

2. Methods 2.1. Canopy model CANOAK is a canopy-scale biophysical model developed by Dennis Baldocchi that computes carbon, water, and energy exchange (fluxes) between the biosphere and atmosphere, integrating concepts from micrometeorology, biochemistry, and ecophysiology. It has been grounded and applied to a number of field sites against measured fluxes (eddy covariance systems) over a range of timescales, predominantly in temperate regions (Baldocchi and Harley, 1995) (Baldocchi, 1997) (Baldocchi and Meyers, 1998) (Baldocchi and Wilson, 2001). Rigorous validation of CANOAK against flux measurements suggests that modelers are correctly parameterizing ecosystem processes while indicating phenomena unaccounted for by the model. While plant physiology has evolved significantly, it is likely that the processes simulated are valid in palaeoecological settings or conversely, can suggest specific evolutionary adaptations that may have occurred to confound our assumptions. The model is driven by meteorological data in hourly steps (air temperature, [CO2], incoming radiation, etc.), simulates radiative transport through the canopy, to then compute the energy balance through multiple layers of leaf and soil to estimate fluxes of sensible and latent heat (Paw, 1987). This also determines proportions of ‘sunlit’ and ‘shaded’ leaves and their respective leaf temperature profiles. A key ecosystem parametrization used in this study that is neglected in regional studies is the encoding of vertical resolution within the canopy, which has been shown to significantly improve the fidelity of computed fluxes (Smith et al., 2010). A simplified flow of processes used by CANOAK is shown in Fig. 1, based on a version by Baldocchi and Wilson (2001). The Farquhar model for photosynthesis (eq. (1) and (2)) (Farquhar et al., 1980) was used in combination with the Ball-BerryCollatz model for stomatal regulation (eq. (3)) (Collatz et al., 1991):

A ¼ Vc  0:5Vo  Rd ;

(1)


Vc  0:5Vo ¼ min Wc ; Wj ð1  G=Ci Þ;

(2)

where A is the rate of photosynthesis, Vc is the rate of carboxylation, Vo is the rate of oxygenation, and Rd is the rate of dark respiration. In eq. (2), min (Wc,Wj) is the minimum between Wc, the rate of carboxylation when Ribulose Biphosphate (RuBP) is saturated and

Fig. 1. Flow of submodules used by CANOAK to compute carbon, energy, and microclimatic profiles.

Wj, the rate of carboxylation when limited by electron transport (low light conditions). The compensation point (G) is the CO2 mole fraction where carbon uptake equals carbon loss, and Ci is the intercellular CO2 mole fraction. Stomatal conductance (gs) can be expressed as a linear function of photosynthesis (A) through eq. (3), for a given relative humidity (rh). The parameters m and g0 are the respective slope and intercept that are fitted against leaf-level gas exchange experiments (Collatz et al., 1991).

gs ¼ mArh=Cs þ g0

(3)

The system of equations coupling photosynthesis and stomatal conductance was embedded in a cubic equation and solved analytically within CANOAK (Baldocchi, 1994). Photosynthesis, respiration, and transpiration are calculated for each leaf layer and then summed for net ecosystem exchanges (Baldocchi, 1994). This computational flow is iterated for each time step until stable values of microclimate, carbon and energy fluxes are reached. Soil and bole respiration are treated using empirical functions while intra-canopy mixing is driven by a turbulent transfer submodule. Soil respiration was set to a constant rate of 6 mmol/m2 s based on recent studies of similar sites (Luo and Zhou, 2006) (Adachi et al., 2009). Comprehensive descriptions of the model and its underlying theory can be found in (Baldocchi and Meyers, 1998) (Baldocchi et al., 2002) (Monson and Baldocchi, 2014). A central concept used in this study is the canopy energy balance (Paw, 1987). The energy balance of an ecosystem describes the flows of incoming, outgoing, and stored energy, serving as the interface between the environment and the surface, which in this case is a forest canopy. Solar radiation drives this system and is either reflected, transmitted, or absorbed, depending on the canopy's spectral properties. Whatever is absorbed is then partitioned into latent heat (evapotranspiration), sensible heat (advection), or

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longwave emission (blackbody radiation), dissipating energy that is otherwise stored primarily by raising surface temperatures. A small amount of solar radiation fuels biochemical reactions that store energy as carbohydrates, used to fuel physiological processes and effectively feed the entire ecosystem (Campbell and Norman, 2012). The integration of these physical and biological processes (ex. radiative transport, energy balance partitioning, photosynthesis) add depth and realism to the simulated canopy, which we show can be the root of certain glacial forest feedback mechanisms. A deeper understanding of these mechanisms allows us to better gauge potential consequences of climatic change as well as get more insight into potential biological and evolutionary implications of changing environmental pressures. 2.2. Climate data and ecosystem parameters Modern climate data and eddy covariance measurements of carbon, water and energy were collected from the Large Scale Biosphere-Atmosphere Experiment in Amazonia (LBA) (Hutyra et al., 2007a) (Hutyra et al., 2007b). One month of hourly aggregated data for February 2003 was taken from continuous measurements of climatic variables and fluxes from a meteorological tower in Tapajos forest in North Central Brazil. Measurements from this data set present a mean air temperature of 24.3 ± 1.9 C, mean vapor pressure of 2.8 ± 0.7 kPa, a monthly cumulative precipitation of 225 mm, and CO2 concentration of 388 ± 12 ppm, reflecting hot and humid modern climate as well as a recent local measurement of atmospheric CO2. Estimates for diffuse photosynthetically active radiation (PAR) were computed through an algorithm by Conghe Song of University of North Carolina at Chapel Hill, based on work by Weiss & Norman and Spitters (Spitters et al., 1986) (Weiss and Norman, 1985). Leaf area index (LAI) was similarly taken from the LBA study while an estimate for carboxylation capacity (Vc;max ¼ 29 mmol/ m2 s), which dictates photosynthetic rates, was taken from Kattge (Kattge et al., 2009) based on the classification of tropical vegetation on oxisol soils. LAI is a dimensionless parameter defined as leaf area (single-sided) per unit ground area (m2/m2) and is a common measure for canopy-density and active biomass, and therefore integral in flux computations. Modifications made for LGM settings were largely based on estimates from Mayle et al. (2009), which gave an overall assessment of likely vegetative changes during the LGM based on an assimilation of pollen and charcoal data with LGM modeling studies. Temperature was uniformly decreased by 5 C (20%) relative to modern data. Atmospheric carbon concentration was set to 200 ppm. These values fall within the mid-range of Cowling's extreme and conservative estimates of LGM conditions (Cowling et al., 2001). Though precipitation was estimated to be 50% lower, modifications were not made in this study as it does not impact flux calculations in CANOAK. It is noteworthy that seasonal precipitation patterns, particularly the severity and length of the dry season have strong impact on the phenology and carbon cycle of tropical forests. 3. Results and discussion 3.1. Validation and LGM carbon processes To ground the model, we applied CANOAK to carbon fluxes in modern Amazonia, as studies on tropical ecosystem-level fluxes are limited relative to those on temperate ecosystems (Dai et al., 2004) (Simon et al., 2005) (Mercado et al., 2009). The primary model output being validated is net ecosystem exchange (NEE), which is defined as the gross primary productivity minus ecosystem

respiration. Eddy covariance towers are equipped precisely to measure NEE at the ecosystem level. Our results will focus on the responses of the competing processes of respiration and photosynthesis to environmental conditions. Model predictions of NEE tend to agree with eddy covariances measurements, estimating mean diurnal patterns within an assumed error of 20% of flux measurements (Fig. 2a) (Moncrieff et al., 1996) (Baldocchi and Meyers, 1998). Model-measurement regression tests between computed and measured fluxes suggest that CANOAK accounts for approximately 86% of the variance in carbon fluxes (Fig. 3), exceeding the community standard of modelmeasurement agreement (r2 > 0:80) (Baldocchi and Wilson, 2001). A significant portion of disagreement stems from nighttime fluxes, when there is no light to drive radiation and the ecosystem simply respires (upper right region of Fig. 3). Though nighttime respiration will play a role in our results, emphasis will be put on modeling the photosynthetic responses that occur during daytime. To explore potential carbon fluxes during glacial periods, the model was then driven by data modified to reflect the colder, lower [CO2] of LGM scenarios. CANOAK estimated a somewhat expected result; less net carbon is exchanged under glacial conditions. The average daytime rate of NEE driven by glacial settings is 56% of computed modern values (52% of measured values). Peak rates of glacially driven NEE are approximately 60% of modern values. A natural conclusion upon first inspection may be that modern tropical climates are closer to ideal conditions for plant growth and that downscaling biologically relevant climatic variables leads to a proportional reduction of net carbon uptake. We performed a factorial experiment with respect to the temperature and [CO2] to investigate their impacts in isolation and in concert. The effects of reduced [CO2] and cooler temperatures act in opposition to one another with respect to carbon fluxes at the ecosystem level, according to our results (Fig. 2b). Reducing the concentration of carbon dioxide from 388 ppm to 200 ppm reduces average daytime NEE to 40% of their modern values and average peak rates to 50% relative to modern rates. This implies that net rates of carbon uptake are indeed sensitive to [CO2] within the tested range of values, which is unsurprising given the body of work from laboratory studies (Sage et al., 1989) (Luo et al., 1996). Reducing average air temperature from 24.3 C (modern) to 19.3 C (LGM scenario) resulted in an 8% increase in average daytime NEE. Hence our model results suggest that cooler LGM temperatures slightly enhance carbon sequestration. To find the origin of this effect, we used CANOAK to test the responses of canopy photosynthesis and canopy respiration to air temperature individually. A larger range of air temperatures were used to study the broader sensitivity of carbon processes to temperature. Computations of canopy respiration rates increased with average air temperature. Respiration typically doubles for a 10 C increase in temperature or is scaled through an Arrhenius function (eq. (4)) used to model the dependence of reaction rates with temperature (Baldocchi and Harley, 1995) (Malhi et al., 1999):

f ðTk Þ ¼ f ð298Þ$exp½ðTk  298ÞHa =RTk 298;

(4)

where f ðTk Þ is the value of the temperature-dependent parameter at temperature Tk in Kelvin, R is the gas constant (0.00831 kJ/mol) and Ha is the activation energy (kJ/mol) for the parameter f. Computations for photosynthesis produced a parabolic dependence on temperature, showing an increase with temperature until it peaks at approximately 19 C. Beyond this, photosynthesis steadily decreases with higher air temperatures. The estimated relationship between air temperature and carbon uptake is largely a product of the Farquhar equations and the modeled temperature-dependence of photosynthetically relevant parameters by Arrhenius functions

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Fig. 2. a Daily averages of Net Ecosystem Exchange at hourly intervals computed by CANOAK, driven by modern data and LGM-adjusted meteorological data, with reference to measured values from an eddy covariance system. b Theoretical computations of carbon flux driven by modern data with independently lowered (LGM) CO2 and temperature.

employed by CANOAK (Sharpe and DeMichele, 1977) (Baldocchi and Harley, 1995) (Hikosaka et al., 2006). This pattern is consistent with other studies on the effects of leaf temperature on photosynthesis, though optimal temperature and sensistivity varies with biomes, species, and even seasons (Baldocchi, 1997) (Roy et al., 2001). The net effect of canopy photosynthesis and respiration as functions of temperature result again in a parabolic relationship where temperature positively correlates with net productivity, an inflection point or ‘plateau’ occurs, after which higher temperatures

reduce net productivity (Fig. 4). Our studies suggest that this inflection point in behaviour could potentially occur between glacial and modern tropical temperatures. While this may seem lower than typical values of peak productivity, it is important to note that air temperature only indirectly affects biochemical processes and it is leaf temperature that is more biologically relevant. It is the energy balance of the leaf that determines leaf temperature and helps elucidate the complex energetic and physiological processes of the leaf.

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Fig. 3. Regression test between model output driven by modern values and measured values of Net Ecosystem Exchange with the equation for the line of best fit and regression coefficient.

Fig. 4. The dependence and sensitivity (slope) of average hourly rates of canopy photosynthesis (carbon uptake) and respiration (carbon release) to air temperature. Rates of canopy photosynthesis and respiration are averaged over the entire day, including nighttime values where rates of photosynthesis are zero. Note that we use the convention of photosynthesis to be a negative carbon flux.

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3.2. Mechanisms behind carbon uptake enhancement 3.2.1. Canopy energy balance The energy balance of the canopy is central in determining energy, water and carbon fluxes. To better understand the behaviour of photosynthesis and respiration rates in the air temperature range between glacial and modern scenarios, we investigated the underlying processes of latent and sensible heat exchange between the canopy and atmosphere. Sensible and latent heat daytime values were averaged for eight scenarios of modified temperatures, including the LGM and modern cases. Sensible heat tends to decrease with increasing average air temperature while latent heat tends to increase with equal but opposite magnitude and sensitivity, obeying conservation of energy given a consistent proportion of longwave emission (Fig. 5a). In the absence of latent and sensible heat fluxes (infinite resistances and zero conductances), CANOAK predicts leaf temperatures upward of 42 C, which would be biologically destructive. We can then interpret latent and sensible heat fluxes as modes to which solar energy can be dissipated to mitigate plant temperature warming (Mahan and Upchurch, 1988) (Michaletz et al., 2015). As radiation is absorbed by the canopy, leaf temperatures increase beyond the thermal equilibrium held with ambient air. This creates a thermal gradient between the air and leaves, inducing the flow of sensible heat exchange (H), which is proportional to the difference between leaf temperature (Tleaf) and air temperature (Tair) such that,

H ¼ rCp

Tleaf  Tair rH

(5)

where r is the air density, Cp is the heat capacity of air, and rH is the boundary layer resistance. Heat loss through long wave radiation also begins to increase dramatically due its quartic dependence on temperature. The remaining proportion of energy is released through latent heat to maintain energy balance. Three distinct ‘regions of sensitivity’ of latent and sensible heat to air temperature were observed (Fig. 5a). The first region occurs in cooler temperatures (T <18 C), the second zone ranges between tropical glacial and modern temperatures (18 C 24 C). Both latent and sensible heat show an increase in sensitivity as average air temperature increases, with all three zones in ranges relevant to modern, palaeo, and predictive contexts. As air temperature rises, sensible heat becomes increasingly suppressed, demanding an increasing amount of compensatory latent heat exchange. Latent heat (lE) is driven by the difference between saturation vapor pressure at leaf temperature (es ðTleaf Þ) and the saturation vapor pressure at air temperature (es ðTair Þ) such that,





rC es Tleaf  es ðTair Þ lE ¼ p g rw

(6)

where g is the psychometric constant and rw is the sum of boundary layer and stomatal resistances. Latent heat flux is thus expressed as the difference between two exponential functions. This function is non-linear, increasing within our range of values, and begins to dominate at higher ambient air temperatures, assuming a constant humidity. At these higher temperatures, stomata tend to close (decrease in stomatal conductance) to temper excessive evapotranspiration. This is an indirect negative effect on productivity (Lloyd and Farquhar, 2008b), which is also dependent on stomatal conductance given that atmospheric carbon is drawn

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into the leaf through the same stomata used for evapotranspiration. The partitioning of energy fluxes is encoded in the solution to the leaf energy balance equation (Paw, 1987) and is independent from tissue damage induced reductions in productivity that occurs at significantly higher temperatures. We propose that it is stomatal closure (Lloyd and Farquhar, 2008b) caused by increased tropical temperatures ( > 19 C) that causes net losses in canopy productivity within our model. 3.2.2. Sunlit and shaded leaf temperatures Leaf temperature, determined by the canopy energy balance, impacts fluxes in a number of ways more conspicuous when using a canopy-scale model such as CANOAK. The radiative transport module, which simulates light penetration through foliage, divides the canopy into ‘sunlit’ and ‘shaded’ leaves along with their respective temperature profiles. Incident solar radiation at each of the leaf layers is also computed, driving photosynthesis as well as energy balance and leaf temperature. Model results indicate that for a number of scenarios, mean leaf temperatures (average of sunlit and shaded leaves) are close to air temperature, while sunlit leaf temperatures tend to be 3e4 C higher (Fig. 5b). Accurate estimation of leaf temperature is vital in flux models, as sunlit leaves are the chief source of photosynthesis, which is dependent on leaf temperature through scaling of biological parameters by Arrhenius functions. We propose that in glacial scenarios with cooler air temperatures, sunlit leaf temperatures and consequently carbon uptake, were bolstered closer to optimal levels through radiative heating. The daytime shaded fraction of leaves does not receive radiative heating and photosynthesizes at a lower rate relative to sunlit leaves, only receiving diffuse (non-direct) photosynthetically active radiation (Monson and Baldocchi, 2014). The entire nighttime canopy does not perform photosynthesis nor receive radiative heating. Both categories of shaded leaves equilibrate with the cooler air temperatures in glacial tropical settings and the accompanied lowered rates of respiration, buffering carbon losses. Analogous effects would also apply to other sources of carbon emission such as bole and soil respiration, which have shown strong temperature dependence. Another salient effect occurs when average monthly air temperature approaches modern values, where leaf temperature actually sinks below air temperature due to heavy rates of evapotranspiration. This phenomena has been observed and studied at diurnal scales in forests and crops largely in the context of plant thermoregulatory mechanisms (Mahan and Upchurch, 1988) (Jones and Rotenberg, 2011) (Dong et al., 2016). Modeling results of this study interestingly reproduce this ‘crossover’ temperature point (Fig. 5b) close to the range of observed values (Tair z 24 C), predicting its presence at larger scales and offering insight into its causal mechanism. As air temperature rises, sensible heat exchange is reduced and latent heat exchange (evapotranspiration) increases in proportion, otherwise driving leaf temperatures to biologically deleterious levels. The ‘cross-over point’, where mean leaf temperature equals air temperature (Fig. 5b), occurs near modern values of average air temperature. At higher air temperatures, sensible heat fluxes approach zero and become negative (Fig. 5a), indicating a reversal of thermal gradient direction and heat flow. Thus, beyond the cross-over point, sensible heat begins to flow from the warmer air to the cooler leaves (Andrews et al., 1992) (Jones and Rotenberg, 2011). Sensible heat would then reverse its direction, now flowing from the hot air toward the cooler canopy. Between LGM and modern air temperatures, sensible heat and latent heat exchange intersect and become equal in magnitude (Fig. 5a). The slopes of sensible and latent heat exchange increase in

Fig. 5. a The dependence and sensitivity of sensible and latent energy fluxes to air temperature. b The dependence and sensitivity of sunlit and mean leaf temperature to air temperature. Note that the ‘cross-over’ point, when the mean leaf temperature sinks below air temperature, occurs near modern temperatures.

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magnitude at modern air temperature values, indicating an increase in sensitivity of heat fluxes to air temperature, and corresponds to the air temperature where the crossover phenomena occurs. This effect could be detected by eddy covariance or Bowen ratio systems and could serve as an ecophysiological alarm, as suggested by Dong et al. (2016). With rising air temperatures, the cross-over point signals an enhanced sensitivity of energy balance partitioning to temperature and increasingly heavy evapotranspirative demand. 3.3. Effects on glacial Amazonia The dominant cause of productivity losses in tropical forests during glaciations is lowered [CO2] according to our study. This has been suggested by global and regional scale modeling experiments (Cowling et al., 2001) (Claussen et al., 2013) (Oishi and Abe-Ouchi, 2013) and has been estimated at the canopy-scale through our study by testing its effects in isolation and interactively with temperature. A marked decrease of NEE (
50% relative to modern) associated with reductions in [CO2], suggests high sensitivity of carbon uptake to substrate concentration over glacial-interglacial cycles. This estimated reduction in carbon fluxes adds to modeling results by Beerling and Mayle (2006) that estimated glacial carbon storage to be approximately half of modern values. This result also aligns with Cowling's regional modeling study of glacial Amazonia that suggested that canopy density, a likely proxy for the magnitude of carbon processes, showed considerable heterogeneity and lower LAI under lower LGM [CO2] (Cowling et al., 2001). Thus, glacial Amazonia had a closed yet thinner and more variable canopy, with a significantly reduced carbon pool, and smaller carbon fluxes, relative to modern Amazonia. These effects could underlie glacial forests' vulnerability to intruding grasslands in marginal areas and more subtle biome shifts to tropical dry forest throughout the basin (Pennington et al., 2000) (Pennington et al., 2004). The robustness of tropical forests over glacial cycles can be attributed to the effects of cooler air temperatures. The effects driven by air temperature are mediated by the canopy energy balance. Colder glacial air temperatures of tropical regions induce high rates of sensible heat exchange, reducing latent heat exchange and evapotranspirative losses considerably. This also reduces the demand for water from the roots, decreasing sensitivity to drought. Colder air temperatures simultaneously lead to reduced ecosystem respiration rates, while sunlit photosynthetically active leaf temperatures are bolstered by radiative heating. At higher interglacial air temperatures, sensible heat exchange decreases as latent heat increases. Stomata in turn respond by closing and consequently inhibit photosynthesis, resulting in a relatively low optimal ambient air temperature that maximizes canopy productivity. Air temperature, through its indirect effect on the stomatal conductance of the sunlit fraction of the canopy, limits photosynthesis in tropical forests which curbs uptake beyond approximately 20 C. This value is somewhat lower than expected for tropical regions but is in agreement with studies in boreal system, which show photosynthesis to rise with temperature until an optimal value, followed by a distinct decrease at higher temperatures (Dang et al., 1997a) (Dang et al., 1997b) (Dang et al., 1998). While optimal values may vary amongst biomes, the fundamental mechanism is consistent. In summary, colder air temperatures in isolation bring about a canopy with a slightly greater ability for carbon uptake while requiring less water and yield a higher water-use efficiency (WUE). This is an oft-used metric in agricultural and forestry that quantifies ecosystem carbon-water relations, defined as the ratio of units of water consumed to units of carbon sequestered. Given lower rates

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of precipitation and water availability, a higher WUE could be critical in maintaining carbon stores, thereby maintaining a closed canopy. Lower rates of precipitation during the LGM may have also resulted in less nutrient leaching and higher soil nutrition relative to modern soils, further aiding forest cover. These types of ecosystem level feedbacks, more often of focus in ecophysiology and carbon modeling, likely have a collective effect on biome stability (Lenton and Lovelock, 2001) with respect to environmental change, helping offset larger detrimental condition such as greatly decreased [CO2]. Thus, our results advance previous claims of improved plant carbon-water relations due to glacial cooling by establishing several underlying, ecophysiological mechanisms. 3.4. Adaptation and dry forest Haffer's Refugia theory and Cowling's canopy-density hypothesis both suggest allopatric speciation as a mechanism for Amazonian biodiversity and explore the effects of respective biome and canopy-structure heterogeneity at regional scales (Haffer, 1969) (Cowling et al., 2001) (Cowling, 2004). Simulating the ecosystem at the canopy-scale can offer us sharper insight into evolutionary processes during the Pleistocene. Large scale climatic changes translate to more local environmental changes that are felt by biota. In the case of forests, these changes are largely mediated by the canopy, which feeds and houses its myriad of organisms. Modeling and phylogenetic studies have proposed the respective expansion and diversification of tropical dry forest over Quaternary climatic oscillations (Beerling and Mayle, 2006) (Richardson et al., 2001). Tropical dry forest species tend to be a drought-tolerant subset of rain forest species. As the climate became colder and drier, these species could flourish and further adapt to aridity. These adaptations could include a deeper root system, defenses against herbivory, changes in stomatal density, an inverse phenology, or physiological changes to leaves in the canopy (Sanchez-Azofeifa et al., 2013). Based on our study, warmer air temperatures, as associated with interglacial periods, induce relatively high rates of evapotranspiration (latent heat exchange) and low rates of sensible heat exchange. These warmer air temperatures also correspond to lower rates of photosynthesis, with the net effect of less efficient watercarbon relations with respect to glacial tropical air temperatures. The thickness of the leaf boundary layer (aerodynamic resistance) is a function of leaf size and shape and ultimately moderates rates of sensible heat exchange. Assuming sunlit leaves are warmer than the ambient air, maximization of sensible heat exchange would buffer evapotranspirative losses. This form of thermal stress would select for thinner, smaller leaves, particularly in the hotter, heavily transpiring upper canopy. Conversely, during glacial periods, leaf morphology could potentially shift to optimize radiative heating effects to boost leaf temperatures closer to their optimal value. At the canopy-scale, empirical studies have argued that species diversity and more directly, functional diversity, has an inverse relationship with evaporation (Baldocchi, 2005). The species composition and structure of foliage in the canopy has also been proposed to optimize photosynthesis, favoring a diverse set of species (Hector, 2011) (Gamfeldt et al., 2013) (Hikosaka and Anten, 2012). This would lead to an increasingly robust and diverse canopy driven by glacial-interglacial cycles. Plants are capable of biochemical, physiological, and structural adjustments when exposed to extended environmental change, which can significantly affect their ecophysiological relationships (Smith and Dukes, 2013). This process is called acclimation. Unlike adaptation, which occurs over multiple generations of taxa, acclimation can occur within an organism's lifespan. The fertilization

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and downregulation of photosynthesis in response to elevated [CO2] (Leakey et al., 2009) and acclimation through variable stomatal sensitivity (Lin et al., 2012) may have a significant impact on carbon, water, and energy fluxes. Acclimation to temperature and [CO2] were not included in this study and should be considered in forthcoming palaeoecological and future modeling experiments to better assess long-term ecosystem response to climatic change. 3.5. Implications for future forests Our modeling results suggests that the air temperatures of modern tropical forests are higher than their optimal value for net carbon uptake. As sensible heat becomes increasingly suppressed by rising air temperatures, evapotranspiration must compensate to cool the canopy, requiring ample supply of water. The sensitivity of evapotranspiration to air temperature is highest in this environment, exceeding the aforementioned ‘cross-over’ point where sensible heat exchange becomes negative. This is accompanied by reduced carbon uptake due to stomatal closure that occurs to subdue excessive evapotranspirative losses. Fertilization due to increased atmospheric carbon dioxide may well-compensate for temperature-related losses, but the net response after acclimation is likely complex and worthy of further study (Lloyd and Farquhar, 2008a). Acclimation to rising air temperatures could also increase the optimal temperature for photosynthesis (Smith and Dukes, 2013), potentially leading to more efficient plant carbon-water relations. In the case where there is insufficient water for cooling, the canopy may experience dessication and burning, leading to thinning and decreases in pool size. The severity of these effects would also be determined by changes in precipitation and would be naturally worsened by drought. 4. Conclusion In this study, we were able to successfully apply a new class of model to an important palaeoecological question: ‘How did Amazonia maintain forest cover through glaciations?’ Initial results are consistent with previous studies at larger scales, estimating carbon uptake to be lower under LGM conditions. Lower atmospheric carbon was found to be the sole cause of reduced ecosystem fluxes, while colder air temperature slightly enhances carbon uptake in the context of LGM Amazonia. This was suggested to be partially rooted in the ‘refrigeration’ of the shaded and night canopy by glacial cooling along with the solar heating of the sunlit, photosynthesizing portion of the daytime canopy. Furthermore, glacial air temperatures in the tropics were suggested to be close to ideal for photosynthesis, where higher temperatures result in stomatal closure to suppress water losses. Finally, analysis of the canopy energy balance through glacial-interglacial periods provides a probable mechanism for improved glacial carbon-water relations. An unexpected but fortuitous result was computation and development of the ‘cross-over’ point, where leaf temperatures sinks below air temperature. This effect may be significant for ecosystem thermoregulation and future response of tropical systems to temperature elevation and should be further investigated. To better characterize the increased aridity on the Amazonia lowland forests over glacial-interglacial cycles using a canopy-scale model, we recommend the inclusion of an integrated soil moisture and precipitation module. Another avenue of improvement would be the examination of vapor pressure changes due to precipitation and its effects on canopy processes. The significance of radiative transfer through the canopy has been assessed in vegetation

models (Huntingford et al., 2008) (Loew et al., 2014), but has yet to be applied in the context of palaeoecology. A Dynamic Global Vegetation Model (DGVM) with a vertically resolved canopy (Clark et al., 2011) could be used to assess the effects of impact of a thermally heterogeneous canopy on carbon fluxes in LGM Amazonia at the regional scale. CANOAK is the integration of a well-established body of theory, grounded against the strongest ecosystem flux measurements available. Using this model enables better usage of modern ecophysiology and hopefully more communication between distinct scientific communities. While palaeo work benefits from records of both climatic change and ecological consequence, it is limited in terms of completeness and resolution. Modern experiments operate at a higher degree of experimental control, but are limited to relatively short timescales. We aim for further synthesis of these approaches to better comprehend the relationship between climates and ecosystems. Acknowledgments Special thanks to Dennis Baldocchi, Young-Lan Shin, Anna Phillips, Vasa Lukic, William Feng, Ting Zheng, Kinoko Sama and Wataru Yamori for helpful discussions and advice through this project. Thank you to my family and friends for love and support through this project. AFunding: This research was supported by the Natural Sciences and Engineering Research Council of Canada, Jeanne F. Goulding Fellowship, Centre for Global Change Science (CGCS) at the University of Toronto and a collaborative Dimensions of BiodiversityBIOTA grant supported by FAPESP (2012/50260-6), NSF and NASA. References Adachi, Minaco, Ishida, Atsushi, Bunyavejchewin, Sarayudh, Okuda, Toshinori, Koizumi, Hiroshi, 2009. Spatial and temporal variation in soil respiration in a seasonally dry tropical forest, Thailand. J. Trop. Ecol. 25. Andrews, P.K., Chalmers, D.J., Moremong, M., 1992. Canopy-air temperature differences and soil water as predictors of water stress of apple trees grown in a humid, temperate climate. J. Am. Soc. Hortic. Sci. 117 (3), 453e458. Baldocchi, D.D., 1994. An analytical solution for coupled leaf photosynthesis and stomatal conductance models. Tree Physiol. 14, 1069e1079. Baldocchi, D.D., 1997. Measuring and modelling carbon dioxide and water vapour exchange over a temperate broad-leaved forest during the 1995 summer drought. Plant, Cell Environ. 20, 1108e1122. Baldocchi, D.D., 2005. The role of biodiversity on the evaporation of forests. In: Forest Diversity and Function. Springer, Berlin Heidelberg, pp. 131e148. Baldocchi, D.D., Harley, P.C., 1995. Scaling carbon dioxide and water vapor exchange from leaf to canopy in a deciduous forest: model testing and application. Plant, Cell Environ. 18, 1157e1173. Baldocchi, D.D., Meyers, T.P., 1998. On using eco-physiological, micrometeorological and biogeochemical theory to evaluate carbon dioxide, water vapor and gaseous deposition fluxes over vegetation. Agric. For. Meteorology 90, 1e26. Baldocchi, D.D., Wilson, K.B., 2001. Modeling CO2 and water vapor exchange of a temperate broadleaved forest across hourly to decadal time scales. Ecol. Model. 142, 155e184. Baldocchi, D.D., Wilson, K.B., Gu, L., 2002. How the environment, canopy structure and canopy physiological functioning influence carbon, water and energy fluxes of a temperate broad-leaved deciduous forestan assessment with the biophysical model CANOAK. Tree Physiol. 22 (15e16), 1065e1077. Beerling, D.J., Mayle, F.E., 2006. Contrasting effects of climate and CO2 on Amazonian ecosystems since the last glacial maximum. Glob. Change Biol. 12 (10), 1977e1984. Burbridge, R.E., Mayle, F.E., Killeen, T.J., 2004. Fifty-thousand-year vegetation and climate history of noel kempff mercado national park, bolivian Amazon. Quat. Res. 61 (2), 215e230. Bush, M.B., Oliveira, P.E.D., 2006. The rise and fall of the Refugial Hypothesis of Amazonian speciation: a paleoecological perspective. Biota Neotropica 6 (1), 0e0. Bush, M.B., De Oliveira, P.E., Colinvaux, P.A., Miller, M.C., Moreno, J.E., 2004. Amazonian paleoecological histories: one hill, three watersheds. Palaeogeogr. Palaeoclimatol. Palaeoecol. 214 (4), 359e393. Campbell, G.S., Norman, J.M., 2012. An Introduction to Environmental Biophysics. Springer Science & Business Media. Clark, D.B., Mercado, L.M., Sitch, S., Jones, C.D., Gedney, N., Best, M.J., Boucher, O., 2011. The Joint UK Land Environment Simulator (JULES), model description-Part

H. Sato, S.A. Cowling / Quaternary Science Reviews 171 (2017) 38e47 2: carbon fluxes and vegetation dynamics. Geosci. Model Dev. 4 (3), 701. Claussen, M., Selent, K., Brovkin, V., Raddatz, T., Gayler, V., 2013. Impact of CO2 and climate on Last Glacial maximum vegetationa factor separation. Biogeosciences 10, 3593e3604. Colinvaux, P.A., De Oliveira, P.E., Bush, M.B., 2000. Amazonian and neotropical plant communities on glacial time-scales: the failure of the aridity and refuge hypotheses. Quat. Sci. Rev. 19 (1), 141e169. Collatz, G.J., Ball, J.T., Grivet, C., Berry, J.A., 1991. Regulation of stomatal conductance and transpiration: a physiological model of canopy processes. Glob. Change Biol. 5, 45e46. Cowling, S.A., 2004. Tropical forest structure: a missing dimension to Pleistocene landscapes. J. Quat. Sci. 19 (7), 733e743. Cowling, S.A., Maslin, M.A., Sykes, M.T., 2001. Paleovegetation simulations of lowland Amazonia and implications for neotropical allopatry and speciation. Quat. Res. 55 (2), 140e149. Dai, Y., Dickinson, R.E., Wang, Y.P., 2004. A two-big-leaf model for canopy temperature, photosynthesis, and stomatal conductance. J. Clim. 17 (12), 2281e2299. Dang, Q.L., Margolis, H.A., Coyea, M.R., Sy, M., Collatz, G.J., 1997. Regulation of branch-level gas exchange of boreal trees: roles of shoot water potential and vapor pressure difference. Tree Physiol. 17 (8e9), 521e535. Dang, Q.L., Margolis, H.A., Sy, M., Coyea, M.R., Collatz, G.J., Walthall, C.L., 1997. Profiles of photosynthetically active radiation, nitrogen and photosynthetic capacity in the boreal forest: implications for scaling from leaf to canopy. J. Geophys. Res. Atmos. 102 (D24), 28845e28859. Dang, Q.L., Margolis, H.A., Collatz, G.J., 1998. Parameterization and testing of a coupled photosynthesisstomatal conductance model for boreal trees. Tree Physiol. 18 (3), 141e153. Dong, N., Prentice, I.C., Harrison, S., Song, Q., Zhang, Y., 2016. Biophysical homeostasis of leaf temperature: a neglected process for vegetation and land-surface modelling. Glob. Ecol. Biogeogr. (under review). Farquhar, G.D., von Caemmerer, S., Berry, J.A., 1980. A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 149, 78e90. Gamfeldt, L., Snll, T., Bagchi, R., Jonsson, M., Gustafsson, L., Kjellander, P., Mikusiski, G., 2013. Higher levels of multiple ecosystem services are found in forests with more tree species. Nat. Commun. 4, 1340. Haberle, S.G., Maslin, M.A., 1999. Late quaternary vegetation and climate change in the Amazon basin based on a 50,000 year pollen record from the Amazon fan, ODP site 932. Quat. Res. 51 (1), 27e38. Haffer, J., 1969. Speciation in Amazonian forest birds. Science 165 (3889), 131e137. Hector, A., 2011. Ecology: diversity favours productivity. Nature 472 (7341), 45e46. Hikosaka, K., Anten, N.P., 2012. An evolutionary game of leaf dynamics and its consequences for canopy structure. Funct. Ecol. 26 (5), 1024e1032. Hikosaka, K., Ishikawa, K., Borjigidai, A., Muller, O., Onoda, Y., 2006. Temperature acclimation of photosynthesis: mechanisms involved in the changes in temperature dependence of photosynthetic rate. J. Exp. Bot. 57 (2), 291e302. Huntingford, C., Fisher, R.A., Mercado, L., Booth, B.B., Sitch, S., Harris, P.P., Harris, G.R., 2008. Towards quantifying uncertainty in predictions of Amazon dieback. Philosophical Trans. R. Soc. B Biol. Sci. 363 (1498), 1857e1864. Hutyra, L., Wofsy, S., Saleska, S., 2007. LBA-ECO CD-10 CO2 and H2O eddy flux data at km 67 tower site, Tapajos national forest. Data Set. Available on-line. Oak Ridge National Laboratory Distributed Active Archive Center, Oak Ridge, Tennessee, U.S.A. http://dx.doi.org/10.3334/ORNLDAAC/860. http://daac.ornl.gov. Hutyra, L.R., Munger, J.W., Saleska, S.R., Gottlieb, E., Daube, B.C., Dunn, A.L., Wofsy, S.C., 2007. Seasonal controls on the exchange of carbon and water in an Amazonian rain forest. J. Geophys. Res. Biogeosciences 112 (G3). Jones, H.G., Rotenberg, E., 2011. Energy, Radiation and Temperature Regulation in Plants. eLS. Kattge, J., Knorr, W., Raddatz, T., Wirth, C., 2009. Quantifying photosynthetic capacity and its relationship to leaf nitrogen content for global-scale terrestrial biosphere models. Glob. Change Biol. 15, 976991. Leakey, A.D., Ainsworth, E.A., Bernacchi, C.J., Rogers, A., Long, S.P., Ort, D.R., 2009. Elevated CO2 effects on plant carbon, nitrogen, and water relations: six important lessons from FACE. J. Exp. Bot. 60 (10), 2859e2876. Lenton, T.M., Lovelock, J.E., 2001. Daisyworld revisited: quantifying biological effects on planetary selfregulation. Tellus b. 53 (3), 288e305. Lin, Y.S., Medlyn, B.E., Ellsworth, D.S., 2012. Temperature responses of leaf net photosynthesis: the role of component processes. Tree Physiol. 32 (2), 219e231. Lloyd, J., Farquhar, G.D., 2008. Effects of rising temperatures and [CO2] on the physiology of tropical forest trees. Philosophical Trans. R. Soc. B Biol. Sci. 363 (1498), 1811e1817. Lloyd, J., Farquhar, G.D., 2008. Effects of rising temperatures and [CO2] on the physiology of tropical forest trees. Philosophical Trans. R. Soc. Lond. B Biol. Sci. 363 (1498), 1811e1817. Loew, A., van Bodegom, P.M., Widlowski, J.L., Otto, J., Quaife, T., Pinty, B., Raddatz, T., 2014. Do we (need to) care about canopy radiation schemes in DGVMs? Caveats and potential impacts. Biogeosciences 11, 1873e1897. Luo, Y., Zhou, X., 2006. Soil Respiration and the Environment. Elsevier/Academic Press, Amsterdam.

47

Luo, Y., Sims, D.A., Thomas, R.B., Tissue, D.T., Ball, J.T., 1996. Sensitivity of leaf photosynthesis to CO2 concentration is an invariant function for C3 plants: a test with experimental data and global applications. Glob. Biogeochem. Cycles 10 (2), 209e222. Mahan, J.R., Upchurch, D.R., 1988. Maintenance of constant leaf temperature by plantsI. Hypothesis-limited homeothermy. Environ. Exp. Bot. 28 (4), 351e357. Malhi, Y., Baldocchi, D.D., Jarvis, P.G., 1999. The carbon balance of tropical, temperate and boreal forests. Plant, Cell & Environ. 22 (6), 715e740. Marchant, R., Boom, A., Behling, H., Hooghiemstra, H., Melief, B., Geel, B.V., Wille, M., 2004. Colombian vegetation at the Last Glacial Maximum: a comparison of modeland pollenbased biome reconstructions. J. Quat. Sci. 19 (7), 721e732. Marchant, R., Berro, J.C., Behling, H., Boom, A., Hooghiemstra, H., 2006. Colombian dry moist forest transitions in the Llanos Orientalesa comparison of model and pollen-based biome reconstructions. Palaeogeogr. Palaeoclimatol. Palaeoecol. 234 (1), 28e44. Mayle, F.E., Burbridge, R., Killeen, T.J., 2000. Millennial-scale dynamics of southern Amazonian rain forests. Science 290 (5500), 2291e2294. Mayle, F.E., Burn, M.J., Power, M., Urrego, D.H., 2009. Vegetation and fire at the last glacial maximum in tropical South America. In: Sylvestre, F., Vimeux, F., Khodri, M. (Eds.), Past Climate Variability in South America and Surrounding Regions: from the Last Glacial Maximum to the Holocene. Developments in Paleoenvironmental Research (14). Springer, New York, ISBN 9789048126729, pp. 89e112. Mercado, L.M., Lloyd, J., Dolman, A.J., Sitch, S., Patino, S., 2009. Modelling basin-wide variations in Amazon forest productivityPart 1: model calibration, evaluation and upscaling functions for canopy photosynthesis. Biogeosciences Discuss. 6 (2), 2965e3030. Michaletz, S.T., Weiser, M.D., Zhou, J., Kaspari, M., Helliker, B.R., Enquist, B.J., 2015. Plant thermoregulation: energetics, traitenvironment interactions, and carbon economics. Trends Ecol. Evol. 30 (12), 714e724. Moncrieff, J.B., Malhi, Y., Leuning, R., 1996. The propagation of errors in long term measurements of land atmosphere fluxes of carbon and water. Glob. Change Biol. 2, 231e240. Monson, R., Baldocchi, D., 2014. Terrestrial Biosphere-atmosphere Fluxes. Cambridge University Press. Mourguiart, P., Ledru, M.P., 2003. Last glacial maximum in an Andean cloud forest environment (Eastern Cordillera, Bolivia). Geology 31 (3), 195e198. Oishi, R., Abe-Ouchi, A., 2013. Influence of Dynamic Vegetation on Climate Change and Terrestrial Carbon Storage in the Last Glacial Maximum. Oliveira, P.E., 1992. A Palynological Record of Late Quaternary Vegetational and Climatic Change in Southeastern Brazil. PhD dissertation. Ohio State University, Colombus. Paw, U.K.T., 1987. Mathematical analysis of the operative temperature and energy budgets. J. Therm. Biol. 12, 227e233. Pennington, R.T., Prado, D.E., Pendry, C.A., 2000. Neotropical seasonally dry forests and Quaternary vegetation changes. J. Biogeogr. 27 (2), 261e273. Pennington, R.T., Lavin, M., Prado, D.E., Pendry, C.A., Pell, S.K., Butterworth, C.A., 2004. Historical climate change and speciation: neotropical seasonally dry forest plants show patterns of both Tertiary and Quaternary diversification. Philosophical Trans. R. Soc. Lond. B Biol. Sci. 359 (1443), 515e538. Richardson, J.E., Pennington, R.T., Pennington, T.D., Hollingsworth, P.M., 2001. Rapid diversification of a species-rich genus of neotropical rain forest trees. Science 293 (5538), 2242e2245. Roy, J., Mooney, H.A., Saugier, B. (Eds.), 2001. Terrestrial Global Productivity. Academic Press. Sage, R.F., Sharkey, T.D., Seemann, J.R., 1989. Acclimation of photosynthesis to elevated CO2 in five C3 species. Plant Physiol. 89 (2), 590e596. Sanchez-Azofeifa, A., Powers, J.S., Fernandes, G.W., Quesada, M. (Eds.), 2013. Tropical Dry Forests in the Americas: Ecology, Conservation, and Management. CRC Press. Sharpe, P.J., DeMichele, D.W., 1977. Reaction kinetics of poikilotherm development. J. Theor. Biol. 64 (4), 649e670. Simon, E., Meixner, F.X., Rummel, U., Ganzeveld, L., Ammann, C., Kesselmeier, J., 2005. Coupled carbon-water exchange of the Amazon rain forest, II. Comparison of predicted and observed seasonal exchange of energy, CO2, isoprene and ozone at a remote site in Rondnia. Biogeosciences Discuss. 2 (2), 399e449. Smith, N.G., Dukes, J.S., 2013. Plant respiration and photosynthesis in globalscale models: incorporating acclimation to temperature and CO2. Glob. Change Biol. 19 (1), 45e63. Smith, W.K., Vogelmann, T.C., Critchley, C. (Eds.), 2010. Photosynthetic Adaptation: Chloroplast to Landscape, vol. 178. Springer Science & Business Media. Spitters, C.J.T., Toussaint, H.A.J.M., Goudriaan, J., 1986. Separating the diffuse and direct component of global radiation and its implications for modeling canopy photosynthesis Part I. Components of incoming radiation. Agric. For. Meteorology 38 (1e3), 217e229. Weiss, A., Norman, J.M., 1985. Partitioning solar radiation into direct and diffuse, visible and near-infrared components. Agric. For. meteorology 34 (2e3), 205e213.