ArticlePDF Available
PNAS 2023 Vol. 120 No. 15 e2301914120 of 2
Canopy-top measurements do not accurately quantify
canopy-scale leaf thermoregulation
JosefC.Garena,1 , LuizaMariaT.Aparecidob, BenjaminW.Blonderc, MollyA.Cavalerid, MartijnSlote,
and SeanT.Michaletza
Leaf traits and climate interact via energy budgets, enabling
leaf temperature (Tleaf) to depart from ambient air tempera-
ture (Tair) (1). When quantied as the slope β of Tleaf vs. Tair,
three types of thermoregulatory behavior are possible: lim-
ited homeothermy (β < 1), poikilothermy (β = 1), and megath-
ermy (β > 1) (2). Characterizing thermoregulation across the
entire leaf area of real-world plant canopies remains an
important challenge for Earth systems science, as Tleaf is a
primary driver of carbon and water uxes.
Recently, Still et al. (3) contributed an important dataset
that advances our understanding of leaf thermoregulation.
Canopy-top thermal imaging data spanning entire growing
seasons at six forested sites across North and Central America
Author aliations: aDepartment of Botany and Biodiversity Research Centre, University of
British Columbia, Vancouver BC V6T 1Z4, Canada; bSchool of Earth and Space Exploration,
Arizona State University, Tempe, AZ 85287; cDepartment of Environmental Science, Policy,
and Management, University of California at Berkeley, Berkeley, CA 94720; dCollege
of Forest Resources and Environmental Science, Michigan Technological University,
Houghton, MI 49931; and eSmithsonian Tropical Research Institute, Panama City 0843-
03092, Republic of Panama
Author contributions: J.C.G. performed research; J.C.G. and S.T.M. analyzed data; M.A.C.
provided data; and J.C.G., L.M.T.A., B.W.B., M.A.C., M.S., and S.T.M. wrote the paper.
The authors declare no competing interest.
Copyright © 2023 the Author(s). Published by PNAS. This article is distributed under
Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND).
1To whom correspondence may be addressed. Email:
Published April 3, 2023.
Fig.1. Relationships between leaf and air temper-
ature along a vertical prole in a tropical wet forest
canopy. Leaf and air temperatures were measured
in Luquillo, Puerto Rico at heights within the canopy
of (A) 2 m, (B) 6 m, (C) 9 m, (D) 12 m, (E) 16 m, and
(F) 20 m (top of canopy). Points represent leaf and
air temperatures averaged in 30-min intervals.
Colors correspond to the density of observations,
with warmer colors indicating more observations.
Solid lines show major axis (Model II) regression,
with slope values (β), corresponding CIs, and r2
values reported in each panel. Dashed line is 1:1.
Full description of the site and data may be found
in Miller etal. (6).
Downloaded from by on April 3, 2023 from IP address
2 of 2
all exhibited β > 1, leading the authors to conclude that limited
homeothermy does not occur in forest canopies.
However, canopy-top thermal imaging does not tell the
full story of leaf thermoregulation. Due to the high infrared
absorptance of water, the foremost leaves in view dominate
infrared signals received by radiometers. These signals
largely exclude lower canopy leaves, which generally com-
prise most of the leaf area (4) and contribute substantially
to gross primary production (5) in forest canopies. Solar radi-
ation dominates the energy balance of upper-canopy leaves,
which are more likely to exhibit midday depression that
reduces transpiration and increases Tleaf (4). Subcanopy
leaves are largely shielded during these periods due to the
“parasol eect” (4, 6) and microclimate buering (7) of the
canopy. Thus, radiometers mounted above canopies as in
Still et al. primarily measure sun-exposed, upper-canopy
leaves and are unable to describe thermoregulation across
the entire canopy.
To demonstrate variation in leaf thermoregulation
throughout a forest canopy, we reanalyzed the time series
of Tleaf and Tair along a vertical prole of a tropical wet forest
in Puerto Rico (6). In these data, only canopy-top leaves (20 m
height) exhibited megathermy (β > 1; Fig. 1). Leaves at 2, 9,
and 12 m exhibited limited homeothermy (β < 1), while those
at 6 and 16 m exhibited poikilothermy (β = 1). Importantly,
Tair was measured at the same heights as Tleaf in this study.
Using Tair from outside the canopy, as in Still et al., would
further increase the apparent homeothermy in lower canopy
layers. Thus, despite observed megathermy in the upper
canopy, most lower canopy layers exhibited limited homeo-
thermy (Fig. 1), thus maintaining leaf temperatures closer to
photosynthetic optima (5). This is consistent with prior work
showing generally reduced Tleaf and dierent thermoregula-
tion strategies in lower canopy layers (8, 9). Further, limited
homeothermy has been observed even in sun-exposed
upper-canopy leaves during certain times of day and in
colder environments (10).
Though we applaud Still et al.’s contribution to our under-
standing of leaf thermoregulation, our analyses suggest that
thermoregulation may be common throughout forest cano-
pies. Accurately quantifying leaf thermoregulation requires
techniques that go beyond relating average canopy-top Tleaf
to Tair. Whole-canopy vertical leaf temperature distributions,
though dicult to measure, will improve our understanding
of why dierent thermoregulation behaviors occur and the
attendant eects on ecosystem functioning.
1. S. T. Michaletz et al., The energetic and carbon economic origins of leaf thermoregulation. Nat. Plants 2, 16129 (2016).
2. B. Blonder, S. T. Michaletz, A model for leaf temperature decoupling from air temperature. Agric. For. Meteorol. 262, 354–360 (2018).
3. C. J. Still et al., No evidence of canopy-scale leaf thermoregulation to cool leaves below air temperature across a range of forest ecosystems. Proc. Natl. Acad. Sci. U.S.A. 119, e2205682119 (2022).
4. N. Vinod et al., Thermal sensitivity across forest vertical profiles: Patterns, mechanisms, and ecological implications. New Phytol. 237, 22–47 (2023).
5. L. He et al., Changes in the shadow: The shifting role of shaded leaves in global carbon and water cycles under climate change. Geophys. Res. Lett. 45, 5052–5061 (2018).
6. B. D. Miller, K. R. Carter, S. C. Reed, T. E. Wood, M. A. Cavaleri, Only sun-lit leaves of the uppermost canopy exceed both air temperature and photosynthetic thermal optima in a wet tropical forest. Agric. For.
Meteorol. 301–302, 108347 (2021).
7. P. De Frenne et al., Global buffering of temperatures under forest canopies. Nat. Ecol. Evol. 3, 744–749 (2019).
8. S. Fauset et al., Differences in leaf thermoregulation and water use strategies between three co-occurring Atlantic forest tree species. Plant Cell Environ. 41, 1618–1631 (2018).
9. A. Rey-Sánchez, M. Slot, J. Posada, K. Kitajima, Spatial and seasonal variation in leaf temperature within the canopy of a tropical forest. Clim. Res. 71, 75–89 (2016).
10. B. Blonder, S. Escobar, R. E. Kapás, S. T. Michaletz, Low predictability of energy balance traits and leaf temperature metrics in desert, montane, and alpine plant communities. Funct. Ecol. 34, 1882–1897 (2020).
Downloaded from by on April 3, 2023 from IP address
... We thank Garen et al. (1) for their comment and agree that there are many issues related to plant thermoregulation that require further study. We do not dispute that our thermal imaging (2) primarily measured the temperature of upper-canopy leaves (T can ) at our sites, and we support additional vertical leaf temperature (T leaf ) studies in various forest types to better understand the microclimate and metabolism of shade leaves. ...
Full-text available
Rising temperatures are influencing forests on many scales, with potentially strong variation vertically across forest strata. Using published research and new analyses, we evaluate how microclimate and leaf temperatures, traits, and gas exchange vary vertically in forests, shaping tree and ecosystem ecology. In closed-canopy forests, upper-canopy leaves are exposed to the highest solar radiation and evaporative demand, which can elevate leaf temperature (Tleaf ), particularly when transpirational cooling is curtailed by limited stomatal conductance. However, foliar traits also vary across height or light gradients, partially mitigating and protecting against the elevation of upper-canopy Tleaf . Leaf metabolism generally increases with height across the vertical gradient, yet differences in thermal sensitivity across the gradient appear modest. Scaling from leaves to trees, canopy trees have higher absolute metabolic capacity and growth, yet are more vulnerable to drought and damaging Tleaf than their smaller counterparts, particularly under climate change. In contrast, understory trees experience fewer extreme high Tleaf 's but have fewer cooling mechanisms and thus may be strongly impacted by warming under some conditions, particularly when exposed to a harsher microenvironment through canopy disturbance. As the climate changes, integrating the patterns and mechanisms reviewed here into models will be critical to forecasting forest-climate feedbacks.
Full-text available
Understanding and predicting the relationship between leaf temperature ( T leaf ) and air temperature ( T air ) is essential for projecting responses to a warming climate, as studies suggest that many forests are near thermal thresholds for carbon uptake. Based on leaf measurements, the limited leaf homeothermy hypothesis argues that daytime T leaf is maintained near photosynthetic temperature optima and below damaging temperature thresholds. Specifically, leaves should cool below T air at higher temperatures (i.e., > ∼25–30°C) leading to slopes <1 in T leaf / T air relationships and substantial carbon uptake when leaves are cooler than air. This hypothesis implies that climate warming will be mitigated by a compensatory leaf cooling response. A key uncertainty is understanding whether such thermoregulatory behavior occurs in natural forest canopies. We present an unprecedented set of growing season canopy-level leaf temperature ( T can ) data measured with thermal imaging at multiple well-instrumented forest sites in North and Central America. Our data do not support the limited homeothermy hypothesis: canopy leaves are warmer than air during most of the day and only cool below air in mid to late afternoon, leading to T can / T air slopes >1 and hysteretic behavior. We find that the majority of ecosystem photosynthesis occurs when canopy leaves are warmer than air. Using energy balance and physiological modeling, we show that key leaf traits influence leaf-air coupling and ultimately the T can / T air relationship. Canopy structure also plays an important role in T can dynamics. Future climate warming is likely to lead to even greater T can , with attendant impacts on forest carbon cycling and mortality risk.
Full-text available
Leaf energy balance may influence plant performance and community composition. While biophysical theory can link leaf energy balance to many traits and environment variables, predicting leaf temperature and key driver traits with incomplete parameterizations remains challenging. Predicting thermal offsets ( δ , T leaf − T air difference) or thermal coupling strengths ( β , T leaf vs. T air slope) is challenging. We ask: (a) whether environmental gradients predict variation in energy balance traits (absorptance, leaf angle, stomatal distribution, maximum stomatal conductance, leaf area, leaf height); (b) whether commonly measured leaf functional traits (dry matter content, mass per area, nitrogen fraction, δ ¹³ C, height above ground) predict energy balance traits; and (c) how traits and environmental variables predict δ and β among species. We address these questions with diurnal measurements of 41 species co‐occurring along a 1,100 m elevation gradient spanning desert to alpine biomes. We show that (a) energy balance traits are only weakly associated with environmental gradients and (b) are not well predicted by common functional traits. We also show that (c) δ and β can be partially approximated using interactions among site environment and traits, with a much larger role for environment than traits. The heterogeneity in leaf temperature metrics and energy balance traits challenges larger‐scale predictive models of plant performance under environmental change. A free Plain Language Summary can be found within the Supporting Information of this article.
Full-text available
Macroclimate warming is often assumed to occur within forests despite the potential for tree cover to modify microclimates. Here, using paired measurements, we compared the temperatures under the canopy versus in the open at 98 sites across 5 continents. We show that forests function as a thermal insulator, cooling the understory when ambient temperatures are hot and warming the understory when ambient temperatures are cold. The understory versus open temperature offset is magnified as temperatures become more extreme and is of greater magnitude than the warming of land temperatures over the past century. Tree canopies may thus reduce the severity of warming impacts on forest biodiversity and functioning.
Full-text available
Globally shaded leaves contribute to more than a half of the total increase in GPP(7.6 Pg C) for 1982-2016. During 1982-2016, the fraction of shaded GPP increases by 1.1% (p<0.01)in tropical forests, and decreases by 1.4% (p<0.01) and 1.8% (p<0.01)in evergreen needleleaf and deciduous needleleaf boreal forests, respectively, suggesting an ecological niche of certain canopy structure for ecosystems to achieve maximum GPP. Unlike transpiration from sunlit leaves that has a turning point in the trend in 2003, global transpiration from shaded leaves steadily increased at the rate of 34 km3 yr-1(p<0.0001) during 1982-2016. Our study,therefore,suggests that shaded leaves have an increasing role in buffering the adverse impact of climate change and extremes. Further studies are still needed to reduce the uncertainties in reported trends arisen from climate forcing data, leaf area index and land cover and land change products.
Full-text available
Understanding leaf temperature (Tleaf) variation in the canopy of tropical forests is critical for accurately calculating net primary productivity because plant respiration and net photosynthesis are highly sensitive to temperature. The objectives of this study were to (1) quantify the spatiotemporal variation of Tleaf in a semi-deciduous tropical forest in Panama and (2) create a season-specific empirical model to predict Tleaf in the canopy. To achieve this, we used a 42 m tall construction crane for canopy access and monitored the microenvironment within the canopy of mature, 20−35 m tall trees of 5 tropical tree species during the wet and the dry season. Tleaf was correlated to photosynthetic photon flux density (PPFD) in the wet season but not in the dry season, possibly due to seasonal differences in wind speed, physiology, and canopy phenology. A structural equation model showed that Tleaf is best explained by air temperature (Tair) and PPFD in the wet season, whereas in the dry season, Tair alone predicted most of the variation in Tleaf. These results suggest the utility of an empirical approach to estimate Tleaf variability where simple meteoro logical data are available. This approach can be incorporated in future models of vegetation− atmosphere carbon and water exchange models of mature tropical forests with similar seasonality
Tropical forests have evolved under relatively narrow temperature regimes, and therefore may be more susceptible to climatic change than forests in higher latitudes. Recent evidence shows that lowland tropical forest canopies may already be exceeding thermal maxima for photosynthesis. Height can strongly influence both the microclimate and physiology of forest canopy foliage, yet vertical trends in canopy micrometeorology are rarely examined in tropical forests. To improve our understanding of how climatological and micrometeorological conditions affect tropical tree function, we assessed vertical gradients of photosynthetic photon flux density, vapor pressure deficit, air temperature, leaf temperature, and the difference between leaf and air temperature (ΔT) in a Puerto Rican tropical wet forest. Both air temperature and vapor pressure deficit increased linearly with height. Leaf temperature, however, did not significantly differ across the shaded foliage from 0-16 m, while the uppermost layer (20 m) was up to 4°C hotter than the rest of the foliage and up to 5°C hotter than air temperature at the highest radiation intensity. As a result, leaf temperatures in the shaded middle canopy and understory showed nearly poikilothermic behavior (i.e., leaf temperatures = air temperature), while the uppermost canopy strata showed megathermic behavior (i.e., leaf temperatures greater than air temperature), revealing different thermoregulation strategies for sun-lit versus shaded foliage. In addition, the uppermost canopy was the only stratum to exceed mean photosynthetic temperature optima for this site (Topt = 30.2 ± 1.1°C). Because the upper canopy plays a disproportionately large role in whole-forest photosynthesis, continued warming could potentially weaken the tropics’ carbon sink capacity. However, the shaded leaves may be able increase carbon uptake with further warming because they appear to be able to maintain temperatures below photosynthetic optima, possibly with the help of radiation shielding provided by the uppermost canopy layer.
Leaf temperature (T leaf) influences rates of respiration, photosynthesis, and transpiration. The local slope of the relationship between T leaf and T air , β, describes leaf thermal responses. A range of values have been observed, with β < 1 indicating limited homeothermy where T leaf increases at a lower rate than T air , β = 1 indicating poikilothermy where T leaf tracks T air , and β > 1 indicating megathermy where T leaf increasingly exceeds T air. However, theory for variation in β has not been developed. Here we derive an equation for β that predicts how it varies with multiple trait and microenvironment variables. The approach also predicts how maintenance of T leaf away from lethally high values may help explain regulation of stomatal conductance (g S). The work delineates contexts in which each class of leaf thermal response is expected and develops concepts for predicting leaf responses to thermally extreme environments.
Given anticipated climate changes, it is crucial to understand controls on leaf temperatures including variation between species in diverse ecosystems. In the first study of leaf energy balance in tropical montane forests, we observed current leaf temperature patterns on three tree species in the Atlantic forest, Brazil, over a 10‐day period, and assessed whether and why patterns may vary among species. We found large leaf‐to‐air temperature differences (maximum 18.3°C) and high leaf temperatures (over 35°C) despite much lower air temperatures (maximum 22°C). Leaf‐to‐air temperature differences were influenced strongly by radiation, while leaf temperatures were also influenced by air temperature. Leaf energy balance modelling informed by our measurements showed that observed differences in leaf temperature between two species were due to variation in leaf width and stomatal conductance. The results suggest a trade‐off between water‐use and leaf thermoregulation; Miconia cabussu has more conservative water‐use compared to Alchornea triplinervia due to lower transpiration under high vapour pressure deficit, with the consequence of higher leaf temperatures under thermal stress conditions. We highlight the importance of leaf functional traits for leaf thermoregulation, and also note that the high radiation levels which occur in montane forests may exacerbate the threat from increasing air temperatures.