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Canopy-top measurements do not accurately quantify canopy-scale leaf thermoregulation

DOI:10.1073/pnas.2301914120
Authors:
Josef Garen at University of British Columbia
Josef Garen
Luiza Maria Teophilo Aparecido at University of Utah
Luiza Maria Teophilo Aparecido
Benjamin W. Blonder
Benjamin W. Blonder
Benjamin W. Blonder
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Molly Cavaleri at Michigan Technological University
Molly Cavaleri
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PNAS 2023 Vol. 120 No. 15 e2301914120 https://doi.org/10.1073/pnas.2301914120 1 of 2
LETTER
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: josef.garen@botany.ubc.ca.
Published April 3, 2023.
AB
CD
EF
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 https://www.pnas.org by 142.103.165.159 on April 3, 2023 from IP address 142.103.165.159.
2 of 2 https://doi.org/10.1073/pnas.2301914120 pnas.org
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 https://www.pnas.org by 142.103.165.159 on April 3, 2023 from IP address 142.103.165.159.
... 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. ...
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