Adaptive differences in plant physiology and ecosystem
paradoxes: insights from metabolic scaling theory
B R I AN J . E NQU I S T *, ANDR EW J . K E RKHO F F *1 , T RAV I S E . HU XMAN * and
E VAN P. E CONOMO w
*Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, AZ 85721, USA,
wSection of Integrative Biology, University of Texas at Austin, Austin, TX 78712, USA
Abstract
The link between variation in species-specific plant traits, larger scale patterns of
productivity, and other ecosystem processes is an important focus for global change
research. Understanding such linkages requires synthesis of evolutionary, biogeogra-
pahic, and biogeochemical approaches to ecological research. Recent observations reveal
several apparently paradoxical patterns across ecosystems. When compared with warmer
low latitudes, ecosystems from cold northerly latitudes are described by (1) a greater
temperature normalized instantaneous flux of CO2 and energy; and (2) similar annual
values of gross primary production (GPP), and possibly net primary production.
Recently, several authors attributed constancy in GPP to historical and abiotic factors.
Here, we show that metabolic scaling theory can be used to provide an alternative
‘biotically driven’ hypothesis. The model provides a baseline for understanding how
potentially adaptive variation in plant size and traits associated with metabolism and
biomass production in differing biomes can influence whole-ecosystem processes. The
implication is that one cannot extrapolate leaf/lab/forest level functional responses to the
globe without considering evolutionary and geographic variation in traits associated
with metabolism. We test one key implication of this model – that directional and
adaptive changes in metabolic and stoichiometric traits of autotrophs may mediate
patterns of plant growth across broad temperature gradients.
In support of our model, on average, mass-corrected whole-plant growth rates are not
related to differences in growing season temperature or latitude. Further, we show how
these changes in autotrophic physiology and nutrient content across gradients may have
important implications for understanding: (i) the origin of paradoxical ecosystem
behavior; (ii) the potential efficiency of whole-ecosystem carbon dynamics as measured
by the quotient of system capacities for respiration, R, and assimilation, A; and (iii) the
origin of several ‘ecosystem constants’ – attributes of ecological systems that apparently
do not vary with temperature (and thus with latitude). Together, these results highlight
the potential critical importance of community ecology and functional evolutionary/
physiological ecology for understanding the role of the biosphere within the integrated
earth system.
Keywords: allometry, ecosystem constants, functional traits, growth efficiency, invariants, latitudinal
gradient, net primary production, scaling, stoichiometry, temperature response
Received 11 July 2005; revised version received 7 January 2006 and accept 17 January 2006
Introduction
Our understanding of the role that organisms play in
influencing global material and energy cycles is in part
constrained by a lack of knowledge of the relative
influences of both abiotic and biotic features of the
integrated earth environmental system (Osmond et al.,
2004). It is clear, however, that the performance of
autotrophs is critical in influencing ecosystem proces-
sing and dynamics. For example, autotrophic respira-
tion plays a substantial role in governing ecosystem
carbon balance (Field et al., 1992; Ryan et al., 1995).
Correspondence: Brian J. Enquist, e-mail: benquist@u.arizona.edu
1Present address: Department of Biology, Kenyon College, Gambier,
OH 43022, USA.
Global Change Biology (2007) 13, 591–609, doi: 10.1111/j.1365-2486.2006.01222.x
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Integration of basic biochemistry and biophysics of
photosynthesis, whole-plant responses to regional and
global climate, and ecology are essential for developing
a predictive understanding of ecosystem flux (Geider
et al., 2001). Therefore, accurate modeling of the re-
sponse of autotrophic respiration and overall carbon
balance to differing climate regimes is essential to
predict the impacts of the traits that influence plant
metabolism on global carbon budgets.
The overall message from autecological studies is that
physiological and life-history traits of plants vary in
accord with changes in climate and edaphic regimes.
Since the pioneering work of Clausen, Keck and Hiesey
(Clausen et al., 1940) botanists have amassed a large list
of examples of how differing environments select for
unique life histories and physiological traits (Mooney &
Billings, 1961; Klikoff, 1966; Strain, 1966; McNaughton,
1967). Differences in local climate and abiotic regimes
can also act as a filter ‘selecting’ those combinations of
organismal traits that ensure that the organism main-
tains a positive carbon and energy balance (Criddle et al.,
1994; Weiher & Keddy, 1995; McGill et al., 2006). Thus, as
a result of acclimatization and environmental selection
of traits, differing ecosystems tend to be characterized
by plants with unique physiological and life-history
adaptations for that specific environment (Schimper,
1903; Shields, 1950; Mooney, 1977; Reich et al., 1999;
Fonseca et al., 2000; Kleidon & Mooney, 2000; Schippers
et al., 2001; Wright et al., 2001; Nicotra et al., 2002).
Although evidence for physiological and life-history
adaptation is abundant, relatively little is known about
the importance of local adaptations in influencing eco-
system processes across broad scale gradients.
Can adaptive and directional shifts in functional traits
influence ecosystem processes?
Patterns of plant trait variation due to both species
replacements and within-species variation across re-
source and environmental gradients (light, water, nu-
trients, and temperature) are thought to reflect local
adaptation (Reich et al., 2003). For example, within
species, there is a rich literature on acclimation, the
adaptive adjustments of physiology to temperature and
other environmental factors (see Criddle et al., 1994;
Atkin & Tjoelker, 2003; Talts et al., 2004; Atkin et al.,
2005; Galme´s et al., 2005). Between species inhabiting
differing environments, the optimal temperatures for
photosynthesis and overall optimal growth are gener-
ally correlated with the temperature range experienced
by plants during the growing season (Amthor, 1989;
Larcher, 1995; Cunningham et al., 1999; Saxe et al., 2001).
Cold adapted plants tend to have physiological adapta-
tions associated with the rate of metabolism. For exam-
ple, they tend to have higher rates of cellular respiration
and carbon assimilation at a given temperature than
plants grown in warm environments (Will, 2000;
Galme´s et al., 2005; but see Wright et al., 2006). Changes
in respiration often reflects (i) an increase in the poten-
tial rates of respiratory activity per unit mitochondrial
volume (Klikoff, 1966; Miroslavov & Kravkina, 1991) in
addition to; (ii) a change in the proteins and efficiency
of terminal oxidase (Ribas Carbo et al., 2000; Kurimoto
et al., 2004); and (iii) an overall altering of the tempera-
ture dependance of metabolism by changes in biochem-
ical activation energies as measured by the Arrhenius
temperature coefficient (Criddle et al., 1994). In common
garden experiments, plant respiration rates are gener-
ally higher for plants originating colder sites (Mooney,
1963; Criddle et al., 1994; Oleksyn et al., 1998). Acclima-
tion of respiration and photosynthesis strongly suggests
that factors other than reaction kinetics regulate plant
flux. In addition to changes in rates of carbon fluxes
associated with respiration and photosynthesis the effi-
ciency of carbon use (the ratio of organismal net pri-
mary production divided by gross primary production
(NPP/GPP), a measure of what fraction of total carbon
assimilated becomes incorporated into biomass) may
also vary across plants across temperature gradients
(Chambers et al., 2004).
Despite the many examples of physiological adapta-
tion and geographic variation in functional groups, it is
still not clear if such evolutionary and ecological
changes in organismal traits systematically alter large-
scale ecosystem processes (Ackerly & Monson, 2003).
Further, what specific adaptive differences in plant
traits could modify ecosystem processes? Recent ana-
lyses suggest that adaptive variation in traits that
influence plant metabolism can have substantial impact
on the carbon balance of ecosystems (Luo et al., 2001;
Kerkhoff et al., 2005; Wythers et al., 2005). Here, we ask
whether plant physiological adaptation can mediate the
influence of abiotic drivers on ecosystem processes such
as primary production or nutrient cycling across the
globe. We build upon a growing awareness of the
importance of functional traits (see McGill et al., 2006)
by mechanistically emphasizing the fundamental role
of potential variation in organismal physiology, instead
of climate alone, in influencing variability in ecosystem
fluxes (Kerkhoff et al., 2005).
This paper has three objectives:
1. We first highlight a prominent yet paradoxical cross-
ecosystem finding that relates environmental tem-
perature and ecosystem energetics. We show how
this pattern has important implications for under-
standing the response of the biosphere to aspects of
global change. To account for this pattern we review
592 B . J . E NQU I S T et al.
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a novel model for scaling organismal metabolism
from cells to ecosystems that builds upon metabolic
scaling theory (West et al., 1997; Enquist et al., 1998,
2003; Brown et al., 2004; Kerkhoff et al., 2005).
2. Next, we show that a trait-based elaboration of
metabolic scaling theory specifies how directional
shifts in plant traits across latitudinal/temperature
gradients can influence ecosystem behavior. In parti-
cular, recent work by Kerkhoff et al. (2005) highlights
the importance of plant tissue nutrient stoichiometry
and growth efficiency. We provide empirical evi-
dence showing that the growth rates of trees (ad-
justed for average mass) does not appear to vary
significantly and systematically in response to a
broad temperature gradient. This result is consistent
with the Kerkhoff et al. (2005) model indicating that
variation in traits associated with organismal growth
and metabolism, due to selection for increased
growth rates in cold environments, can in turn yield
the ‘paradoxical responses’ of whole-ecosystems
mentioned above.
3. Finally, we explore the implications of an approxi-
mate invariance in growth rate with latitude/
temperature for autotrophic respiration and net eco-
system primary production. Specifically, we show
that the ratio between ecosystem capacities for re-
spiration and net assimilation is invariant with
respect to a temperature gradient, providing one of
several ‘ecosystem invariants.’
Latitude, temperature, and paradoxical patterns of
ecosystem flux and production constants
A physical explanation for large-scale variability
in ecosystem flux along temperature and
latitudinal gradients
Temperature is fundamental in influencing the kinetics
of biochemical reactions. In general, rates of biologically
mediated conversions are tightly linked to changes in
temperature (Johnson et al., 1974; Lloyd & Taylor, 1994).
It is widely thought that increases in global temperature
will bring about increases in the metabolic activity of
organisms within terrestrial ecosystems. Recently, how-
ever, utilizing a network of CO2 and H2O flux monitor-
ing stations across Europe (EUROFLUX), Valentini et al.
(2000) found no trend in annual ecosystem GPP across
European latitudes north of the Mediterranean. Further,
a recent analysis by Kerkhoff et al. (2005) showed that
variation in instantaneous rates of net primary produc-
tivity, showed little to no variation with latitude and
growing season temperature. These results are surpris-
ing as they run counter to the prominent paradigm that
cold, high latitude ecosystems are less productive than
warmer, lower latitude ecosystems (Lieth, 1975).
Valentini et al. (2000) hypothesized that the apparent
constancy in GPP was not due to functional trait or
diversity differences between sites but instead due to
the relatively high abundance of soil carbon and recent
warming of northerly latitudes. However, others have
suggested that there are no clear trends of decreasing
soil carbon with increasing mean annual temperature
(Thornley & Cannell, 2001). In contrast, Kerkhoff et al.
(2005) hypothesized that the relative constancy of in-
stantaneous rates of NPP with temperature was due to
possibly adaptive differences in growth rates across
temperature gradients.
An alternative hypothesis: the three A’s – Acclimation
Adaptation, Assembly – can negate physical drivers of
ecosystem flux and production
The findings of Giardina & Ryan (2000) (Liski et al., 1999)
and Baldocchi et al. (2001) may offer another insight into
the relative insensitivity of GPP and annual NPP
(ANPP) with latitude noted by Valentini et al. (2000)
and Kerkhoff et al. (2005). Giardina & Ryan (2000) found
that soil decomposition rates across a global-scale gra-
dient in mean annual temperature were remarkably
constant. Baldocchi et al. (2001) noted that the tempera-
ture optimum for ecosystem photosynthesis appeared to
change with mean growing season temperature. Similar
to findings from comparative ecophysiology of leaves
(Niinemets et al., 1999), ‘cold’ ecosystems seemed to
have lower temperature optima for photosynthesis and
‘warm’ ecosystems had higher temperature optima
(Fig. 1). The findings from Baldocchi et al. suggest that
photoautotrophic processes may systematically vary
across broad gradients. However, the specific mechan-
isms behind such shifts in the optimum temperature for
ecosystem photosynthesis are not clear. If, as proposed
for autotrophs, whole-ecosystem respiration acclimates
to ecosystem photosynthate supply (i.e. primary pro-
duction; Dewar et al., 1999), then the temperature re-
sponse of whole-ecosystem carbon flux and biomass
production will likely also be altered.
Building upon the findings of Valentini et al. (2000)
and Giardina & Ryan (2000), Enquist et al. (2003) used
data from FLUXNET (http://daac.ornl.gov/FLUXNET/)
to document a related pattern of ecosystem invariance.
Across a variety of arid and mesic sites in both Europe
and North America, CO2 and energy flux was charac-
terized by a similar exponential functional response
with temperature the Boltzmann or Van’t Hoff reac-
tion rate rule (Gillooly et al., 2001). However, when the
total annual ecosystem respiration was plotted as a
function of annual temperature no significant relation-
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ship was found (Fig. 2). More importantly, they found
that when the instantaneous rates of ecosystem respira-
tion were standardized for a given temperature, colder
and higher latitude ecosystems actually exchanged CO2
and energy at three- to sixfold greater rates than war-
mer low latitude ecosystems. Figure 3 shows a positive
correlation between temperature-standardized flux (at
20 1C) and latitude for all sites used in the analysis
(r25 0.569, n5 46, F5 58.06, Po0.0001 data from En-
quist et al., 2003). Enquist et al. concluded that taking the
annualized and instantaneous findings together illus-
trates a paradox – why should it be that (i) there are no
significant differences in annual fluxes across diverse
ecosystems yet (ii) instantaneous fluxes of colder sites
are much greater than warmer sites?
Enquist et al. (2003) provided a mechanistic model to
account for the observed temperature response function
of ecosystem respiration. Based on this model, they
outlined several hypotheses to explain the increase in
instantaneous rates of respiration at a standardized
temperature and the approximate constancy in total
annual respiration across latitude. One possibility
proposed by Enquist et al. is the organismal-centered
hypothesis that focuses on the importance of local
adaptations or acclimation of cellular metabolism
(b0 in the model of Enquist et al., 2003) and turnover
in the presence and relative abundance of species.
Below, we revisit the Enquist et al. (2003) model to
assess the hypothesis that the approximate invariance of
annual ecosystem flux and the increase in the rates of
instantaneous flux across sites (with temperature or
latitude) results from adaptive changes in organismal
metabolism across broad gradients. Focusing more spe-
cifically on the autotrophic community alone, we utilize
Fig. 1 Data from Baldocchi et al. (2001) (Fig. 9) showing a
change in the temperature optimum for CO2 uptake and the
mean summer temperature for several sites in the FLUXNET
dataset. The positive correlation indicates that the photosyn-
thetic temperature response curves of entire ecosystems varies
in direct proportion to the mean growing season temperature
experienced by that ecosystem. ‘Cold ecosystems’ have lower
optimal temperatures for optimum photosynthesis than ‘warm
ecosystems.’ The slope of the line is close to 1.0 indicating that
the ecosystem response in optimal photosynthesis temperature
is closely matches a change in growing season temperature.
Fig. 2 Relationship between the annual night-time CO2 flux
(average rate per second) and the average annual night-time
temperature for several FLUXNET sites. Data from Enquist et al.
(2003). Temperature, T, is plotted as inverse temperature as
measures in kelvins (K). The differing symbol numbers refer to
different sites as originally listed in Enquist et al. (2003). The solid
symbols are for European sites and the open symbols are for
North American sites Numbers on the upper x-axis are tempera-
ture in degrees C.
Fig. 3 Increase in the temperature normalized (at 20 1C) instan-
taneous nightly ecosystem energy flux (Be) with latitude. Note,
temperature normalized data are natural log transformed. The
positive correlation indicates that at a given temperature, high
latitude sites flux energy and carbon at greater rates than low
latitude sites. Sites include all of the site years listed in Enquist
et al. (2003). The dataset is dominated by forest ecosystems
although there are a few grassland and arid sites included.
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a recently modified version of this model (Kerkhoff et al.,
2005) to argue that the above paradoxical variation in
ecosystem fluxes primarily reflects local adaptations
to cooler temperatures and shorter growing seasons that
involve how stoichiometric changes influences plant
metabolism and the efficiency of biomass production.
A general model for scaling organismal metabolisms
from cells to ecosystems
Enquist et al. (2003) utilized metabolic scaling theory
(West et al., 1997; Enquist et al., 1998; Brown et al., 2004)
to derive a general equation for how temperature and
plant size will influence ecosystem flux. Metabolic
scaling theory builds upon the approach advocated
by Harte (2002). Specifically, we take ‘a Fermi approach’
(or a zeroth-order model a la West et al., 1997), in that
our goal is to construct the