LETTER
https://doi.org/10.1038/s41586-018-0582-4
Effects of climate warming on photosynthesis in
boreal tree species depend on soil moisture
Peter B. Reich
1,2
*, Kerrie M. Sendall
1,3
, Artur Stefanski
1
, Roy L. Rich
1,4
, Sarah E. Hobbie
5
& Rebecca A. Montgomery
1
Climate warming will influence photosynthesis via thermal effects
and by altering soil moisture
1–11
. Both effects may be important
for the vast areas of global forests that fluctuate between periods
when cool temperatures limit photosynthesis and periods when
soil moisture may be limiting to carbon gain
4–6,9–11
. Here we show
that the effects of climate warming flip from positive to negative
as southern boreal forests transition from rainy to modestly dry
periods during the growing season. In a three-year open-air
warming experiment with juveniles of 11 temperate and boreal
tree species, an increase of 3.4 °C in temperature increased light-
saturated net photosynthesis and leaf diffusive conductance on
average on the one-third of days with the wettest soils. In all 11
species, leaf diffusive conductance and, as a result, light-saturated
net photosynthesis decreased during dry spells, and did so more
sharply in warmed plants than in plants at ambient temperatures.
Consequently, across the 11 species, warming reduced light-
saturated net photosynthesis on the two-thirds of days with driest
soils. Thus, low soil moisture may reduce, or even reverse, the
potential benefits of climate warming on photosynthesis in mesic,
seasonally cold environments, both during drought and in regularly
occurring, modestly dry periods during the growing season.
A changing climate will influence plants by altering temperature,
precipitation and soil moisture, as well as their variability and sea-
sonality
1–11
. In temperate and boreal climates, temperatures switch
seasonally from cold (and limiting to biological processes) to warm and
periodically dry, during which time moisture can be limiting
2–6,9–11
.
Both the ‘law of the minimum’ and multiple limitation theory
12–14
pro-
vide a conceptual basis for predicting climate warming interactions
with soil moisture. Although higher temperatures may alleviate enzy-
matic limits on the biochemistry of photosynthesis, realized rates of
CO
2
assimilation may decrease if and when low soil water causes sto-
matal closure and limitation of the CO
2
substrate for photosynthesis. As
growing season conditions in temperate and boreal forests are likely to
become effectively drier than in the past
3,8,9
, because climate warming
will increase evapotranspiration more than precipitation
3,9
and increase
variability in the amount of precipitation per event
1,9
, the importance of
water availability to forest responses to rising temperature may increase
in the future
3–6,9–11,15–18
.
Mid- and high-latitude plants will therefore probably experience
both positive and negative effects of climate warming on photosynthe-
sis within and across years—we propose that these will be positive when
soil moisture is ample but negative when soils are drier
4–6,9–11,15–17
.
Whether such effects are in aggregate positive or negative is likely to
depend on the balance of time that warming alleviates low temperature
limitations to plant function as opposed to causing limitations to func-
tion through decreased soil moisture. However, direct tests of the effects
of climate warming across a range of soil moisture conditions, caused
by seasonal or interannual variation or by manipulations of tempera-
ture or moisture, are rare, and it remains unclear how plant responses
to climate warming will be influenced by these indirect effects of soil
moisture
4–6,9–11,16–18
.
Here we provide evidence from 11 co-occurring boreal and temperate
tree species (Fig. 1) in support of the overarching hypothesis that low
soil moisture status has a dampening effect on the photosynthetic
enhancement that results from experimental warming. This moisture
regulation of the response to climate warming was consistent for all 11
species and occurred in response to reductions in soil moisture due
to typical seasonal variation and in response to further reductions
in soil moisture due to experimental warming. Results are from the
free-air B4WarmED experiment
19–22
, in which juveniles (3–5 years old
at the time of measurements) of local ecotypes of the 11 tree species
were grown under ambient and seasonally elevated (+3.4 °C, April–
November) temperatures from 2009 to 2011 at two southern boreal
sites in Minnesota, USA (Extended Data Table 1 and Methods). The
11 species co-occur in forests in northern Minnesota; however, five
are boreal with southern range limits in or near Minnesota and six are
temperate with northern range limits not far north of the Minnesota–
Canada border
19
. Fluctuations in soil moisture levels (volumetric
water content (VWC), m
3
H
2
O per m
3
soil) occurred at both sites and
across all years (Extended Data Fig. 1 and Extended Data Table 2), and
spanned from 0.27 to 0.05 VWC, representing a range from slightly
wetter than field capacity to slightly drier than the permanent wilting
point (of approximately -1.5 MPa) for these sandy loam soils
23,24
. Leaf
temperature (T
leaf
) and vapour pressure gradient (VPG) also varied
considerably across all photosynthetic measurements (Extended Data
Fig. 2).
All species responses were consistent with the hypothesis that effects
of experimental warming on carbon gain would be less positive or
more negative during periods of low soil moisture (Fig. 1, Table 1 and
Extended Data Table 3). In moist soils, all angiosperm species (and
no gymnosperms) showed higher maximum carboxylation capacity
at 25 °C (V
cmax-25
) when grown at increased temperature compared
to ambient temperatures (Extended Data Fig. 3), helping to explain
the higher light-saturated net photosynthesis (A
net
) in warmed plants
when soil water limitations were modest (Fig. 1). This higher maximum
carboxylation capacity in well-watered, warmed angiosperms assessed
at a standardized temperature is indicative of an acclimation response
(upregulation of V
cmax-25
) to growth in elevated temperatures. However,
every species showed marked sensitivity of A
net
to drying soil moisture
(Fig. 1). More relevant to our overarching hypothesis, A
net
in all species
declined more steeply with decreasing soil moisture in warmed than
in ambient conditions (Fig. 1); therefore, when compared at a common
soil moisture, plants showed the most positive (or least negative) effects
of experimental warming on A
net
when soil moisture availability was
high, whereas positive effects decreased (or negative effects increased)
as soil moisture availability declined (Fig. 1).
In other words, we found a significant interaction between
the increased temperature treatment and VWC for A
net
(Table 1;
F
1,553
= 40.9, P < 0.0001) in a model that included treatment (increased
or ambient temperature), species, VWC and two other environmental
drivers (T
leaf
and VPG). Moreover, although species differed from each
other in A
net
, they did not differ in how VWC influenced their response
1
Department of Forest Resources, University of Minnesota, St. Paul, MN, USA.
2
Hawkesbury Institute for the Environment, Western Sydney University, Penrith, New South Wales, Australia.
3
Department of Biology, Georgia Southern University, Statesboro, GA, USA.
4
Smithsonian Environmental Research Center, Edgewater, MD, USA.
5
Department of Ecology, Evolution and Behavior,
University of Minnesota, St. Paul, MN, USA. *e-mail: preich@umn.edu
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