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Linking Plant and Ecosystem Functional Biogeography: A B C D
Linking Plant and Ecosystem Functional Biogeography: A B C D
Edited by Stephen W. Pacala, Princeton University, Princeton, NJ, and approved January 29, 2014 (received for review February 1, 2013)
Classical biogeographical observations suggest that ecosystems One of today’s scientific challenges is to directly link the
are strongly shaped by climatic constraints in terms of their structure observations at organismic and ecosystem levels (21–23) to de-
and function. On the other hand, vegetation function feeds back on velop a profound understanding of biotic interactions with en-
the climate system via biosphere–atmosphere exchange of matter vironmental constraints: i.e., hydrometeorological and nutritional
and energy. Ecosystem-level observations of this exchange reveal preconditions. One fundamental question in this context is to
very large functional biogeographical variation of climate-relevant
what degree the local composition of morphological, anatomical,
biochemical, or physiological features measurable at the indi-
ecosystem functional properties related to carbon and water cycles.
vidual plant (so-called “plant traits”) have an influence on the
This variation is explained insufficiently by climate control and a clas- underlying process chains that may matter for the variation of
sical plant functional type classification approach. For example, corre- ecosystem fluxes and properties (24). The future importance of
lations between seasonal carbon-use efficiency and climate or biogeography for an integrated Earth-system science will crucially
environmental variables remain below 0.6, leaving almost 70% depend on its capacity to inform which plant traits (and their local
of variance unexplained. We suggest that a substantial part of this composites) matter for the spatiotemporal variations of functions
unexplained variation of ecosystem functional properties is related to occurring at the ecosystem scale, in addition to, and independently
variations in plant and microbial traits. Therefore, to progress with of, climate and environmental factors. A biogeography of ecosystem
ENVIRONMENTAL
global functional biogeography, we should seek to understand the functional properties has to explore multiple sources of information,
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link between organismic traits and flux-derived ecosystem properties from species-distribution maps and satellite remote-sensing data to
at ecosystem observation sites and the spatial variation of vegetation local trait and flux observations, and foster the incorporation of
traits given geoecological covariates. This understanding can be fos- biotic observations into process-based models (4, 25). An approach
tered by synergistic use of both data-driven and theory-driven eco- of this kind may allow us to scrutinize the emergent behavior of the
logical as well as biophysical approaches.
local plant communities along with their (nonlinear) responses to,
and collective feedbacks with, the environment.
In this contribution, we review recent advances of functional
biogeochemistry | plant traits | carbon cycle | eddy covariance | FLUXNET biogeography at the ecosystem level as achieved by the global
network of biosphere–atmosphere observation and its integration
ENVIRONMENTAL
tant ecosystem-internal variation of physiology is for the variation
daily time step, one can infer the ecosystem parameter (RUE),
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which is independent of the ecosystem structure embedded in the
fAPAR observation (48, 49). Such an ecosystem-level parameter
links more strongly to ecophysiological parameters in global
Earth-system models (e.g., Vcmax and Jmax in the Farquhar
model) (50, 51). Classically, the ecophysiological parameters in
global vegetation models are assumed constant per each plant
functional type (PFT). These functional types are most often
defined according to leaf habit (broadleaf, needle leaf), longevity
(evergreen, deciduous), and life form (tree, shrub, grass, crop)
and relate to vegetation type at the ecosystem level, which are
defined based on the dominating PFTs (e.g., evergreen broadleaf
forest). Parameterization strategies relying on FLUXNET data
offer the chance to analyze the between- and within-vegetation
type variability of the essential ecosystem parameters. Fig. 2B
shows that there is considerable variation within vegetation types
(here, evergreen needle leaf forest). It remains a challenge to
explain this between-site variability. The within-vegetation type
variability is partly, although not solely, dependent on species
and should be able to be traced back to the traits of the dominant
individuals of the ecosystem.
Obviously, the carbon balance of an ecosystem is determined
not only by the variation of GPP but with the same importance
by processes that determine the mean residence time of the
assimilated carbon in the system: for instance, allocation and
respiration of carbon, as well as disturbance events, such as
fires, that lead to rapid release of carbon (52). Mahecha et al.
(33) have found a convergence of the temperature sensitivity of
ecosystem respiration. However, they found a considerable varia-
tion in the seasonal change of carbon respired versus carbon taken
up: i.e., the seasonal carbon-use efficiency. In other words, some
ecosystems respire a large proportion of the assimilated carbon
within one season whereas others tend to store it. Fig. 3 shows that
little of this variability can be explained by climate or conven-
tional site characteristics. The question is whether the seasonal
carbon-use efficiency belongs to a syndrome of ecosystem func-
tional properties that might be underlying control by plant,
faunal, and microbial traits.
The Potential of Plant Traits for Explaining Ecosystem
Fig. 2. (A) Covariation of net ecosystem production (NEP) with peak light-
Functional Properties
saturated GPP (90%ile) at seven European long-term observation sites [(data The role of plant traits as important determinants of ecosystem
from Lasslop et al. (40)]. (B) Within- and between-species variation of the functioning was recognized early on (29). Ultimately, the concept
Carnegie–Ames–Stanford Approach (CASA) model parameter “maximum of plant functional types is based on the observation that different
light-use efficiency” inferred with a model inversion approach [error bars trait syndromes result in distinct broad differences in ecosystem
indicate SEs; data from Carvalhais et al. (48)]. Compare SI Appendix for more functioning. However, the large within-PFT variability of both
details on analysis and sites. biogeochemical processes (compare the previous section) and trait
Reichstein et al. PNAS | September 23, 2014 | vol. 111 | no. 38 | 13699
the stable N isotope ratio of plant tissues (δ15N) (65) as, e.g.,
obtained from wood samples or herbarium specimens of leaves
(66, 67).
Plant traits related to the water cycle include those affecting
plant water uptake (rooting depth, root mass, and specific root
length), transport (hydraulic properties), storage, and loss (sto-
matal and cuticular conductance, leaf size) and thus should
strongly link to the spatial variation found in Fig. 1A. At the leaf,
plant, and ecosystem scale, water-use efficiency (WUE) can be
derived from the carbon-isotope signatures δ13C of plant tissues
(e.g., leaves, tree rings), which integrate WUE from daily to de-
cadal timescales (68, 69). For trees, wood density has been found
to be an important and well-documented integrative trait related
to hydraulic conductivity, leaf traits (including photosynthetic
ones), and patterns of water uptake and transpiration (70) and is
thus potentially a good proxy for water use and its constraints
on the carbon cycle (Fig. 4). Wood density has also been sug-
gested as an indicator of drought resistance as it is positively
related to cavitation resistance (71). However, a recent study
indicated that, under an extreme drought, species compensated
low wood density by drought deciduousness, higher sensitivity
of stomata to leaf water potential, and possibly also greater
Fig. 3. Seasonal carbon-use efficiency after Mahecha et al. (see figure 3 and
rooting depth (72). Thus, wood density should not be used
online supporting material in ref. 33) in relation to other ecosystem and
without considering other traits when predicting resistance and
climatic characteristics at FLUXNET sites. Shown are histograms of each resilience to extreme drought. Similarly, whereas in all biomes
variable across all sites and their relation with the seasonal carbon-use ef- trees typically operate at a narrow safety margin for vulnerability
ficiency. On top of the panels, the (linear) Pearson correlation coefficient to drought (73), species may differ in their strategy of drought
and the distance correlation coefficient are shown. avoidance and their capacity of xylem refilling (74). This obser-
vation not only reinforces the notion that drought effects on the
carbon cycle may be better captured by a combination of plant
values (18) calls for exploring the joint patterns between these two traits, but also suggests that, in multispecies forests, different spe-
sets of observation. It has been demonstrated that, across different cies may respond at different thresholds and thus may potentially
PFTs and biomes, there is a convergence in the relationships of increase the resistance and resilience of ecosystem processes to
chemical, structural, and physiological leaf traits [the “leaf eco- extreme events.
nomics spectrum” (LES)] (20). While the LES includes some Although it has been argued that functional diversity could be
variation, partly explained by climate, it is robust in permitting the the most relevant measure for ecosystem productivity and sta-
prediction of leaf physiological parameters based on leaf nitrogen bility (75), there is still very limited empirical evidence demon-
concentrations and leaf mass per area (19, 53). Note, however, strating the role of functional trait diversity (which could account
that leaf mass per area (LMA) has recently been suggested to for both inter- and intraspecific variation) (76, 77). Clearly,
reflect primarily its functional relationship with leaf lifespan and targeted studies are needed to explicitly test for such relation-
biases the correlation of leaf traits, which are functionally often ships, as well as the effect of species identity or keystone species.
area-proportional (54). Similarly, wood and root N concentrations Different levels of phylogenetic and spatial integration should be
(and root lifespans) are closely related to wood and root respi- addressed by including specific site-level information and data
ration rates (55, 56) although the slopes may differ between from trait databases (SI Appendix, Fig. S3).
functional groups (e.g., grasses versus legumes) (57). Thus, eco-
system properties, such as GPPsat and the autotrophic component The Ecosystem Is More than the Sum of Traits: Scale
of ecosystem respiration, can be in principle derived from plant Emergent Properties at the Ecosystem Level
traits (Fig. 4). The advantage of investigating data-driven linkages between
The heterotrophic component of ecosystem respiration is vegetation traits and ecosystem functional behavior is its di-
more difficult to approximate from plant traits. However, litter rectness. However, one should not always expect a simple re-
decomposition, which contributes substantially to heterotrophic lation between ecosystem functions and traits at the organismic
respiration in many ecosystems, can be well-predicted from plant level (such as the former being a simple linear combination of
traits such as C, N, dry matter content, and lignin (58–60). Dif- the latter) because ecosystems are complex dynamic and adap-
ferent organs (leaves, stems, roots) exhibit a different, although tive systems that may experience scale emergent properties when
apparently coordinated, behavior (“plant economics spectrum”) one transcends scales (78). For example, the reflectivity of a leaf
(61). Under similar climates, wood decomposition is also well- is not the same as the albedo of a canopy (79). Forest canopies
correlated with nitrogen and phosphorus concentrations and C/N are effective at trapping light so they may appear much darker
ratios, with gymnosperms decomposing more slowly than (at 400- to 800-nm wavelengths) than the reflectivity of in-
angiosperms (62). Through effects on litter quality, plant traits dividual leaves indicates. Nor is the light-use efficiency of a leaf
have also been suggested as important drivers for microbial the same as of a canopy (80, 81). The light-response curve of
community composition and shifts between more strongly sapro- individual plant canopies ranges from being linear for well-
phytic-based to more strongly symbiotic-based C cycling and thus watered crops that form a closed canopy and have high nitrogen
soil organic carbon stabilization (63). Root traits, such as specific inputs (82) to being curvilinear with open canopies and those
length, tissue density, and diameter, are important determinants of limited in nitrogen resources (80). Similarly to leaves that in-
soil C turnover (64) and thus may contribute to the variation of teract regarding the transfer of radiation through the canopy in
carbon-use efficiency (Figs. 3 and 4). Root traits should thus also a way that needs explicit scaling, other ecosystem processes
influence soil N turnover processes although this topic has so emerge from interactions between individuals given their specific
far received little attention. By changing tissue N concen- traits. For example, how strongly physical traits such as leaf
trations and allocation patterns, changes in N availability will toughness will influence the mean-residence time (and thus long-
likely impact plant and ecosystem properties associated with term accumulation) of carbon will depend on the existence of
the carbon cycle (compare to this section, above, and Fig. 4). a decomposer community that might be specialized to digest
An interesting trait reflecting long-term changes in N availability is such material. Often in these contexts, biological symbioses are
Climate
canopy, the processing of the photosynthetically fixed carbon de-
LAI GPPsat R0 pends even more on biological processes that are controlled by
Upscaled maps
Spatial covariates
traits, including allocation, respiration and decomposition, and
Height WUEp stabilization of carbon in the soil. Overall, in the biogeochemical
gs A Ra Earth-system context, the challenge is to explore classical bio-
Plant traits
Species
Leaf size geographical questions from a functional perspective: The question
NUEp
δ13C how to explain spatial patterns of species distribution and diversity
Wood density has to be rephrased as: What are the determinants and bio-
LMA, N, P geochemical consequences of plant functional attribute and trait
Root depth SRL LDMC variation? How do the inter- and intraspecific variability of plant
traits depend on environmental constraints and affect the de-
Soil
Soil C and nutrient turnover (incl. litter decomposition)
rived ecosystem functional properties beyond productivity? How
are response traits and effect traits coupled with ecosystem
Chemical traits
functional properties? Can a combined approach of up-scaled
Structural traits traits and down-scaled fluxes help quantifying emergent prop-
erties across vegetation types and biogeographic regions? Note
Fig. 4. Major relationships between plant structural and chemical–physio- that such emergent properties could comprise, e.g., nonadditive
logical traits and ecosystem functional properties related to carbon and water effects and/or effects induced by the canopy structure and re-
fluxes, embedded in an upscaling framework considering spatial covariates. lated microclimatic conditions (76, 84). What is the role of func-
Tradeoffs related to water-use (WUE), nitrogen-use (NUE), radiation-use tional diversity for ecosystem functional properties and their re-
(RUE), and carbon-use (CUE) efficiencies at plant (p) and ecosystem scale are sistance and resilience to disturbance and long-term environmental
ENVIRONMENTAL
printed in italics in red. Note that soil C and nutrient turnover processes are changes?
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also important ecosystem properties affecting carbon fluxes directly via het- To our mind, a crucial criterion for future progress in this
erotrophic soil respiration and indirectly via effects of nutrient availability on direction will be whether a stronger integration of largely disjoint
plant functional traits and ecosystem structure. A, photosynthetic capacity; activities will be achieved. For example, hypotheses regarding
δ13C, stable carbon isotope ratio; ET, evapotranspiration; GPPsat, gross primary the link between organismic traits and ecosystem flux-derived
productivity at saturating light; gs, maximum stomatal conductance; LAI, leaf whole-ecosystem properties can be best tested if the respective
area index; LDMC, leaf dry matter content; LMA, leaf mass per area; N, tissue observations are made at the same sites. Remote-sensing ap-
nitrogen concentration; NEE, net ecosystem exchange of CO2; P, tissue phos- proaches that have been successful for characterizing ecosystem
phorus concentration; R0, ecosystem respiration at reference temperature; Ra,
structural parameters (e.g., leaf area index) and their effect on
plant respiration; SRL, specific root length.
ecosystem functions need to be extended to detecting plant traits
and their diversity. It has recently been demonstrated that
hyperspectral remote sensing can be a powerful tool for mapping
crucially determining the cycling of elements. Examples include trait syndromes, which could be used for monitoring functional
termite–microbial symbiosis, without which decomposition of shifts in ecosystems (85). Finally, trait-based modeling approaches
lignin would be much retarded in tropical savannahs, or the in- should be linked to the observations via model–data fusion
fluence of ruminant–microbial symbiosis for digesting lichens in approaches, where the biosphere model parameters (i.e., traits)
high-latitude ecosystems. Similarly, a trait related to fast re- can be constrained from the ecosystem-level observation via
sprouting may be very important for ecosystem carbon dynamics model inversion and compared with observed organismic traits.
in a frequently disturbed system, but not necessarily in a more
Once the mechanistic scaling of trait effects on ecosystem functions
stable environment. Therefore, traits are a necessary but not
and response to climate has been successful, such a model would go
sufficient condition to understand the ecosystem carbon balance.
beyond the projection of species and trait maps under changing
It is needed to explicitly explore and model the interactions of
conditions and can inform dynamic Earth-system models to
individuals and to compare the emerging behavior against ob-
served ecosystem functions varying in time and across sites. For calculate effects of changing climate and land use on ecosystem–
an approach applicable at global scale, see ref. 83. atmosphere carbon and energy exchange and related feedbacks (86).
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