Discussion
We examined P dynamics in the plant,
soil and leachate in a humid tropical forest exposed to 7-year of
continuous field warming. Contrary to most studies which show that
short-term warming increases ecosystem P deficiency in arid ecosystems
or large scales (Jonasson et al.,
2004; Yuan & Chen, 2015), we found that warming by 2.1°C
increased plant P uptake and
decreased foliar N:P, indicating warming drove
sustained plant P demand and may
alleviate P deficiency and/or
limitation of enhanced plant growth
and contribute to sustaining plant C fixation in these tropical forests.
It is worth pointing out that the sustained plant P demand could not be
explained by traditional views in accessing P acquisition (through fine
root and mycorrhizal fungi; Rosling et al., 2016) and supply (through P
availability), because neither fine root biomass nor arbuscular
mycorrhizal fungi abundance were affected by 6-year warming as they were
by short-term warming (Lie et al., 2021), and soil soluble P had no
response to warming.
We observed a enhanced P redistribution capacity and soil P mobilization
to support increasing plant P demand without altering litter P
mineralization and leachate P, which led to a net transfer of P from
soil to plant regulated by biogeochemical processes (Fig. 5): (1)
warming increased plant P resorption by 4.7%, which enhanced plant P
recycling and soil P inputs; (2) warming elevated soil
P mineralization by 15.4% and
dissolution by 6.8% in the topsoil, thereby improving soil P supply;
(3) reduced P loss in surface runoff under warming facilitated P
retention for topsoil and shallow roots. Our findings improved the
understanding of biogeochemical controls on plant P acquisition under
warming, which are crucial to project the future C sequestration
potential of tropical ecosystems that are mostly limited by P (Fig.1;
foliar N:P > 20) (Güsewell, 2004; Cleveland et al., 2013).
Plant P resorption increased under warming, similar to observations at
the global scale that plant P resorption was positively correlated with
temperature (Yuan & Chen, 2009; You et al., 2018). Plant growth periods
strongly drive plant nutrient
resorption (Sun et al., 2016). A warming experiment conducted in
subtropical forests showed that foliar growth periods were extended by
an average of 5–18 days at 2°C of warming (Gunderson et al., 2013).
Thus, warming potentially delays
foliar senescence (Chung et al.,
2013) and consequently increases foliar plant P resorption (Estiarte &
Peñuelas, 2015). Moreover, it is noted that plant P resorption increased
with P supply derived from soil (i.e.,enhanced P mineralization and
dissolution) under warming, which contradicts the view on a trade-off
between nutrient resorption and soil nutrient supply
(Vergutz et al., 2012; Gerdol et
al., 2019). We found that increased P resorption was likely driven by
warming-induced drying soil (Fig. S5), which is consistent with a study
in a dry ecosystem (Ren et al., 2018). P resorption increases P-use
efficiency in plants via higher P productivity and longer residence time
of P, while new roots may be limited in the capacity to take up P from
litter in drier soil. Thus, an increase in plant P resorption may be a
more economical P acquisition
strategy than increased investment in roots. These findings
extend
the application of
resorption theory to P cycling, and
also highlight the key P source from resorption for plants under
warming.
Most studies reported that P mineralization in humid forest soils was
enhanced under warming (Rui et al., 2012; Zhou et al., 2013; Zi et al.,
2018; Zuccarini et al., 2020). Consistent with these studies, warming
elevated soil P mineralization by increasing soil potential acid
phosphatase activity and decreasing
moderately-available organic P in topsoil. The elevated soil P
mineralization could be driven by joint increases in plant demand for P
and microbial activity (e.g., higher soil respiration (Li et al.,
2016)). The increase in soil acid phosphatase activity could be
stimulated by microbes to compensate for the reduction of P diffusion in
warming-induced drying soil (Allison et al., 2010) and the limitation of
microbial P utilization during litter decomposition with higher litter
C:P (Table S3; Sardans et al., 2006). Our data thus showed that more P
was retained in plants than returned to soil in each litter cycle under
warming, which led to a net transfer of P from soil moderately-available
organic P to the plant.
At our site, a large fraction of the moderately-available P in the soils
was in inorganic form (>58%), suggesting that inorganic P
dissolution may be especially important for P supply. In line with our
hypothesis, warming enhanced P dissolution, as evidenced by lower Fe-Pi
in the topsoil. However, the Al-Pi and pH in the three soil depths were
not affected by warming, suggesting that the decrease in Fe-Pi was not
caused by soil pH, which served as a critical factor of P dissolution
(Navratil, et al., 2009; Devau et al., 2011). Rather, the lower Fe-Pi
was likely related to sensitive changes of soil Fe phases under warming.
In topsoil, warming led to decreases in redox potential and increases in
both Fe(II)HCl:FeHCl and
Feca concentrations, indicating higher Fe reduction. Our
finding challenges the prevailing expectation that warming drives more
oxidative soil, due to increased soil porosity by warming-induced drying
soil (Wang et al., 2017). The higher Fe reduction probably was due to
the enhanced microbial activity, root respiration coupled to higher P
uptake capacity and thus oxygen depletion under warming at our site (Li
et al., 2016). Compared with Al minerals, the reduction of Fe minerals
is considered to effectively reduce geochemical sequestration of
easily-available P to increase soluble P and even alleviate P limitation
in humid tropical soils (Chacón et al., 2006; Lin et al., 2018; Gross et
al., 2020). Some studies in subtropical wetland systems have reported
similar declines in redox potential and increases in P release from Fe
minerals under warming (Zhang et al., 2012; Wang et al., 2013).
Accordingly, the increases in P release can elevate soil soluble P, as
observed in incubation experiments with higher soluble P under reducing
conditions (Peretyazhko & Sposito, 2005; Wang et al., 2017). However,
we did not find changes in soil soluble P, which might suggest a rapidly
attained equilibrium, in which soluble P induced from the dissolution of
Fe-Pi was rapidly taken up by plants in this P-poor system (Liptzin &
Silver, 2009). The rapid plant uptake could prevent potential P
re-immobilization and loss by leaching. Overall, the increase in P
release from Fe minerals provides evidence for greater soil P supply
under warming, which was expected to facilitate plant P utilization.
The losses of P deserve to be noticed under warming. P in terrestrial
ecosystems is primarily lost through leachate that makes it difficult
its return to the system. Currently, global P mineable reserves are
gradually being lost from ecosystems due to improper use of P
fertilizers in forest and farmland managements. Greater plant P uptake
generally promotes P fixation in plants and thereby potentially reduces
P loss. Intriguingly, we noted that the increased plant P uptake does
not imply less P losses, because the net P losses were counterbalanced
by the decreased P losses in surface runoff and the increased P losses
in underground water. These results suggest that warming shifts P loss
from surface to subsurface, and
emphasizes the necessity to assess
effects of warming on P dynamics at the ecosystem level.
Our study provides new insights into
understanding tropical P cycling processes and modelling forest P
limitation under warming. The findings of
the sustained plant P demand driven
by increasing P supplies through multiple biological and geochemical
processes within the ecosystems (e.g., plant P resorption, soil P
mineralization, and P release from Fe
minerals) under warming extend the
traditional assessment method (measure P supply by available/soluble P)
and the current paradigm states (assess P conversation only by soil P
mineralization). This suggests that previous studies may have
overestimated the impacts of P limitation on ecosystem C stock under at
least short-term or medium-term future warming (Wieder et al., 2015).
Our study also provides additional information on P dynamics that can be
incorporated into earth system models which require further
quantification (Reed et al., 2015; Sun et al., 2017).