University of Groningen
The cost of living
Schmitz, Cordula
IMPORTANT NOTE: You are advised to consult the publisher's version (publisher's PDF) if you wish to
cite from it. Please check the document version below.
Document Version
Publisher's PDF, also known as Version of record
Publication date:
2010
Link to publication in University of Groningen/UMCG research database
Citation for published version (APA):
Schmitz, C. (2010). The cost of living: Temperature compensation of the metabolic rate in plants
Groningen: s.n.
Copyright
Other than for strictly personal use, it is not permitted to download or to forward/distribute the text or part of it without the consent of the
author(s) and/or copyright holder(s), unless the work is under an open content license (like Creative Commons).
Take-down policy
If you believe that this document breaches copyright please contact us providing details, and we will remove access to the work immediately
and investigate your claim.
Downloaded from the University of Groningen/UMCG research database (Pure): http://www.rug.nl/research/portal. For technical reasons the
number of authors shown on this cover page is limited to 10 maximum.
Download date: 16-06-2017
CordulaS-diss
13-09-2010
13:43
Pagina 7
1
Chapter
Introduction
Cordula Schmitz
CordulaS-diss
13-09-2010
13:43
Pagina 8
Chapter 1
The concept of a species can be defined as ‘individuals which resemble each other more
than they resemble anything else’ (De Candolle 1855). This definition of species implies
that species differ in their shape, morphology, structure, anatomy and in their function, the physiology. Nevertheless, species have to deal with similar physical and
chemical constraints, such as gravity, which have an effect on the shape and structure
of animals and plants. By evolutionary processes the properties of plants and animals
are optimized within given constraints.
„[…] preservation of favourable individual differences and variations, and the destruction
of those which are injurious, I have called Natural Selection […]” (Darwin 1859).
As a consequence species are optimized in their shape, structure and function to
their environment, within given constraints from general physical principles. Some of
these optimization principles of species are described by allometric scaling relations.
These relations describe size-dependent differences across the variety of species, but
also for individuals belonging to a single species. A number of allometric scaling relations have been derived, describing e.g. size-dependent variation in the metabolic
activity or growth rate (Rubner 1883; Kleiber 1947; Enquist & Niklas 2002; Niklas &
Enquist 2002; Brown et al. 2004; Marquet et al. 2005; Etienne et al. 2006; O'Connor et
al. 2007).
Optimizing the generation of metabolic energy is important, as it is the fundamental enzymatic process for life, providing the energy supply and reducing equivalents for proper functioning of both a species and the whole ecosystem The total
respiratory requirement of a species is the sum of the growth metabolism, activity
metabolism and basal/maintenance metabolism (Cannell & Thornley 2000).
Differences in growth, activity levels or maintenance costs will result in differences in
metabolic rate (Poorter & Remkes 1990; Bunce & Ziska 1996; Daly & Peck 2000). The
allometric scaling of the basal metabolic rate implies that the relative maintenance
costs differ for differently-sized species.
“The chameleon-like influence of absolute and relative scale is evident whenever we draw
up on an equation derived from the physical sciences to describe a biological feature.”
(Niklas 1994)
On the one hand, bigger organisms, having a higher biomass, have in principle a
higher investment in maintenance, so that the absolute basal metabolic rate is
increased. While on the other hand, with increasing size, the relative investment is
decreased. Therefore, big organisms have a higher absolute basal metabolic rate, but a
lower relative basal metabolic rate compared to small organisms. Such size-dependent
differences in the metabolic rate result from size-dependent differences in the relative
surface, where gases and nutrients can be exchanged. With increasing size, the 2dimensional surface and 3-dimensional volume increase unequally, resulting in a
8
CordulaS-diss
13-09-2010
13:43
Pagina 9
Introduction
decreased surface to volume ratio. Thus the basal metabolic rate (B) should decrease
by a scaling exponent of 2/3, implying that B = Mass2/3 (Kleiber 1947; Rubner 1883).
The Metabolic Theory of Ecology (MTE) presumes that all organisms share an optimized fractal-like transporting network, minimizing hydraulic resistance and maximizing the exchanging surface (West et al. 1997; Brown et al. 2004). The underlying
assumption, that such a fractal-like network is space-filling, has as a consequence, that
the maintenance metabolic rate is related to the surface to biomass ratio of an
organism. Accordingly, the presumed optimization of the transporting network and
the exchange surface leads for all organisms to a scaling of the metabolic rate (B) to
biomass by 3/4: B = Mass 3/4
However, considering different bacteria, fungi, plants and animals, it seems incongruous that the size-dependence of the surface to mass ratio and therefore the change
in relative basal metabolic rate, can be described by one and the same allometric
scaling relation for all species (Makarieva et al. 2005; Apol et al. 2008; White 2010).
Comparing animals to plants, animals have a blood-vessel-system and plants a
vascular network, differing in their branching pattern and construction (Reich 2001).
While it seems reasonable that differences in the relative basal metabolic rate of
animals can be predicted from the increase in the 2-dimensional surface to 3-dimensional biomass, the situation in plants is different. The filigree-like surface of plants,
the leaves and branches, should result in a different size-dependence of the metabolic
rate than the cubes-like size-dependence given for animals. In plants the major above
ground surface area is that of the leaves, so that the relation of leaf area to above
ground biomass reflects the surface to mass ratio. For plants the leaf area to leaf
biomass, the specific leaf area, depends on plant traits and environmental conditions
(Reich et al. 1999; Wright et al. 2005a; Wright et al. 2005b; Poorter et al. 2009). As a
consequence, the allometric scaling of the basal metabolic rate should not apply
strictly for plants.
In addition, size dependent variations in biomass allocation patterns in plants
might impact the maintenance costs. Different tissues differ in their metabolic activity.
The roots and leaves have the high metabolic activity while for woody tissue, such as
the stem of shrubs and trees, the metabolic activity is relatively low. Thus biomass allocation patterns affect whole plant metabolic rate (Poorter et al. 1990; Tjoelker et al.
1999; Niklas & Enquist 2002; McCarthy & Enquist 2007).
Furthermore, temperature has a profound effect on enzymatic reaction rates and is
likely to affect the basal metabolic rate (e.g. Bennett 1972; Feder 1976; Wagner &
Larcher 1981; Barko & Smart 1981; Walsh & Somero 1981; Brechignac & Furbank
1987; Van Iersel 2003; McCarthy & Enquist 2007). If we assume that in all species the
same key-metabolic steps are rate-limiting and catalyzed by the same enzymes, then,
from the thermodynamic effect of temperature on enzymatic reactions, it could be
expected that along a transect from the arctic to the tropics, the basal metabolic rate
would gradually increase together with the ambient temperature. The MTE presumes
that the temperature-dependence of organisms is given by the Arrhenius-term,
9
CordulaS-diss
13-09-2010
13:43
Pagina 10
Chapter 1
describing the temperature-dependent change of enzymatic reaction rates (Gillooly et
al. 2001; Brown et al. 2004): e–E/kT . Here T is the absolute temperature (in Kelvin), E
is the activation energy of the key metabolic-enzymes (in eV) and k is the Boltzmann
constant (8.62 * 10-5 eV/K).
While the biomass-dependence results from evolutionary optimization of morphological properties of organisms, the Arrhenius-term describes the temperature-dependence of the basal metabolic rate in a purely physical manner. It is, however, likely that
evolutionary optimization also affects enzymatic reactions, in such a way that organisms compensate for the thermodynamic effect (Clarke 2003; Clarke 2004; Clarke &
Fraser 2004; Clarke 2006). Optimal maintenance and therefore optimizing the basal
metabolic rate is important as it is typically related to fitness (Parsons 2005; DeWitt et
al. 1998). Therefore, the basal metabolic rate is expected to be optimized in relation to
the temperature in the region of origin. The temperature in different environments
might have an impact on the species-specific maintenance requirements like e.g.
higher parasitism, requiring higher immune defence and therefore a higher basal
metabolic rate (Colditz 2002; Klasing 2004).
Evolutionary optimization could favour a basal metabolic rate that is as low as
possible, to minimize the investment needed for maintenance. However, keeping the
basal metabolic rate minimal could be disadvantageous, e.g. if a higher investment for
immune defence is required. Therefore a minimal basal metabolic rate could negatively impact fitness. In contrast, maximizing the metabolic rate is disadvantageous
when due to ecosystem restrictions and species-specific trades, such as food and
nutrient availability or nutrient use-efficiency, respectively, energy becomes limiting.
Favouring a high basal metabolic rate would result in a waste of resources, which
might be better stored for later use. An optimal basal metabolic rate should be the
result of the balance between species-specific traits and ecosystem limitations. Such a
basal metabolic rate can be related to temperature, in the sense that maintenance
requirements differ between temperatures, but should not be strictly determined by
the effect of temperature on enzymatic reactions.
Adjusting the basal metabolic rate to the temperature in the region of origin is the
result of evolutionary optimization. Evolutionary modifications occur when and an
organism is exposed to a different temperature over generations (Feder 1976; Somero
1978). In addition organisms can adjust within their phenotypic plasticity to variations in temperature during their lifetime by acclimation (e.g. Chatterton et al. 1970;
Tjoelker et al. 1999; Xiong et al. 2000; Hicks & McMahon 2002; Atkin & Tjoelker
2003; Terblanche et al. 2007). The extent and duration of acclimation of the basal
metabolic rate to the prevailing temperature is dependent on the phenotypic plasticity
of an organism (Chatterton et al. 1970; Stamou et al. 1995; Atkin et al. 2000a;
Campbell et al. 2007). Phenotypic plasticity is variable between species, some have a
higher capacity to adjust than others (Sultan 2003; Ghalambor et al. 2007), but also
dependent on life history of an individual (Atkin et al. 2006b). For plants, newly
developed tissue is better adjusted to the current temperature than pre-existing tissue
10
CordulaS-diss
13-09-2010
13:43
Pagina 11
Introduction
developed at a different temperature (Campbell et al. 2007; Ow et al. 2008).
Consequently, the extent a plant can adjust should be related to growth-rate and to the
turnover rates of different tissues, which implies that plants containing a substantial
amount of woody tissue, such as trees and shrubs, with a low turnover rate, can not
adjust as well as herbaceous plants.
Furthermore exposing a plant to a different temperature can be accompanied by a
shift in energy delivering pathways (Amthor 2000; Juszczuk & Rychter 2003). Such a
shift is expected to result from temperature-induced limitation of ADP availability, a
substrate of the mitochondrial electron transport chain (Fader & Koller 1984; Atkin et
al. 2000b). A shift to the alternative oxidase pathway, which is uncoupled from the
ATPsynthase, will lead to lower energy yield per oxygen used. The relation between
ATP (energy) production and measured respiration can thus vary, depending on the
relative use of both respiratory pathways. As the alternative oxidase pathway is
assumed to play a role in the maintenance of growth-rate homeostasis in variable
conditions (Hansen et al. 2002; Moore et al. 2002) and in stress reduction, changes to
low and to high temperature both will stimulate its use (Ow et al. 2008). This temperature-dependent use of the alternative oxidase pathway implies that the Arrhenius
relation between temperature and basal metabolic rate is further relaxed.
The master-equation of the MTE is the combination of the presumed biomass- and
temperature-dependences of the basal metabolic rate of organisms:
B = b0 * M 3/4 * e–E/kT
Where b0 is the species-specific normalization constant, M 3/4 the scaling of the
metabolic rate on biomass and e–E/kT the Arrhenius-term.
“The whole is more than the sum of its parts.” quoted by Aristotle
Expressing the basal metabolic rate as the sum of the biomass- and temperaturedependencies ignores the possibility that the effects of biomass and temperature might
be interdependent variables.
The size- and temperature-dependence of the basal metabolic rate might influence
each other. E.g. temperature-dependent differences in the shape and structure might
counterbalance the thermodynamic effect of temperature. Versa vice, e.g. size might
affect the sensitivity of the metabolic rate to temperature.
The aim of this thesis is to describe the biomass- and temperature-dependence of
the basal metabolic rate of a variety of species (interspecific) and individuals of a
single species (intraspecific) from different thermal environments. Interspecific differences reflect genotypic variations and intraspecific differences show phenotypic variations, which are typically related to the plastic response of species, living in different
thermal environments. Data are obtained from literature surveys, laboratory experiments and field studies.
11
CordulaS-diss
13-09-2010
13:43
Pagina 12
Chapter 1
In Chapter 2 we redefine the temperature-dependence of the basal metabolic rate.
We present a model showing the impact of temperature for different exposure durations: immediate, intermediate and long-term. This model is supported by a metadata
analysis. In addition in Box 1 we highlight how various parameters such as temperature in the region of origin, species-specific differences and biomass affect the shortterm temperature response of the basal metabolic rate.
In Chapter 3 we examine the impact of biomass on the basal metabolic rate of
plants. Besides the surface to biomass ratio, we determine other size-dependent
features of the plant and their relevance for the metabolic rate. In Box 2 we compare
and discuss the intra- and interspecific differences in the leaf area to biomass ratio,
biomass allocation patterns and its impact on the basal metabolic rate.
Subsequently, in Chapter 4 we highlight the effects of extended temperature exposure on the morphology of plants. We examine the effects of phenotypic (intraspecific)
and genotypic variations (interspecific) on physiological compensation and morphological variation in different temperatures. In Box 3 we further show the impact of
temperature-dependent phenotypic variations on a variety of scaling relations.
In Chapter 5 we present a field study on the effect of climate on leaf morphology
and its consequences for the effect of temperature on the basal metabolic rate. In Box
4 we present an additional metadata analysis on the effect of temperature on morphological features.
Finally, Chapter 6 summarizes the temperature- and biomass-dependence of the
metabolic rate, highlighting differences between animals and plants and differences at
the intra- and interspecific level.
12
CordulaS-diss
13-09-2010
13:43
Pagina 13
Introduction
13
CordulaS-diss
13-09-2010
13:43
Pagina 14