Download Effects of Tissue-type and Development on Dark Respiration in Two

Annals of Botany 87: 355±364, 2001
doi:10.1006/anbo.2000.1341, available online at http://www.idealibrary.com on
E€ects of Tissue-type and Development on Dark Respiration in Two Herbaceous
Perennials
C H E RY L L . M C C U TC H A N * and R U S S E L L K . M O N S O N
University of Colorado, Department of Environmental, Organismic and Population Biology, Campus Box 334,
Boulder, CO 80209-0334, USA
Received: 27 July 2000 Returned for revision: 31 August 2000 Accepted: 16 November 2000 Published electronically: 26 January 2001
Perennial plants go through a number of developmental stages during the growing season. Changes in metabolism
during these phases have been documented in laboratory-grown plants but never in native plants growing in natural
habitats. The purpose of this study was to describe the seasonal pattern of dark respiration in the above-ground tissues
of two herbaceous perennials, Bistorta bistortoides (Pursh) Small and Campanula rotundifolia L., growing in the Rocky
Mountains (USA). The e€ect of biomass accumulation on respiration rate and di€erences in respiration rate among
tissues were measured. Respiration rate di€ered signi®cantly among the above-ground tissues. Reproductive structures
had the highest respiration rates, followed by leaves, then stems. Respiration rate decreased by 10±90 % over the
growing season in these tissues but was generally not correlated with a decrease in biomass accumulation. The seasonal
pattern of respiration rate varied signi®cantly among tissues. Total tissue respiratory ¯ux was calculated at 15 8C for
each tissue. In both species, total above-ground respiratory ¯ux was either relatively constant during the growing
season with a marked decrease at seed dispersal or a maximum rate was reached at mid-season. In B. bistortoides, leaves
had the highest total respiratory ¯uxes, and the respiratory ¯uxes of the stem and reproductive structures were similar
to one another. In C. rotundifolia, leaf and stem respiratory ¯uxes were similar, while the respiratory ¯ux of the
reproductive structures was considerably lower than that of leaves and stems. This study emphasizes the importance of
developmental processes and tissue-type on respiration rate and highlights the importance of including all plant tissues
# 2001 Annals of Botany Company
in predictive models of plant carbon balance.
Key words: Respiration, development, growth, maintenance, tissue, Bistorta bistortoides, Campanula rotundifolia,
harebell.
I N T RO D U C T I O N
The carbon lost from respiratory metabolism within an
individual plant has been calculated to be between 30 and
70 % of the carbon gained through photosynthesis (Kimura,
1970; Pate, 1979; Farrar, 1980a; Massimino et al., 1980;
Lambers et al., 1981; Peterson and Zelitch, 1982). In
addition, it accounts for approx. 50 % of the carbon e‚ux
from terrrestrial ecosystems on a global scale (Schimel,
1995). In ecosystem carbon balance models, respiratory
carbon ¯ux must often be calculated with functions that are
based on assumptions rather than empirical evidence. For
example, calculations of respiration are made as a fraction of
canopy photosynthesis or as a function of temperature,
biomass, surface area, or nitrogen content (Agren et al.,
1991; Raich et al., 1991), despite the fact that these and other
factors may interact to alter respiration within plant tissues.
The measurement of natural variation of respiration is
essential for predicting carbon loss from individual plants
and whole ecosystems.
The percentage of photosynthate lost by respiration is
a€ected by plant development, tissue maintenance costs
and biomass allocation to various tissues. These variables
are in turn in¯uenced by environmental variables such as
temperature, light availability and nutrient availability.
* For correspondence at: Institute of Ecosystem Studies, Route 44A,
Box AB, Millbrook, NY, 12545, USA. Fax (845) 677-5976, e-mail
[email protected]
0305-7364/01/030355+10 $35.00/00
Variation in respiration with plant development and among
plant tissues is relatively unstudied in natural populations
of plants. In the past decade, researchers have begun to
characterize the e€ect of these variables on respiration in
deciduous and evergreen tree species (McLaughlin et al.,
1990; Amthor, 1991; Ryan et al., 1995, 1997; Pregitzer et al.,
1998; Bolstad et al., 1999; Clinton and Vose, 1999; Atkin
et al., 2000). Currently, little is known about variation in
respiration rate in natural populations of annuals and
herbaceous perennials which are important understorey
components of forested ecosystems and are the dominant
plants of tundra and grasslands.
In a theoretical sense, we understand that respiratory ¯ux
associated with growth and maintenance costs [as de®ned by
McCree (1970) and Thornley (1970)] should vary among
plant tissues (Penning de Vries, 1975) and be dependent on
tissue function. Several studies have compared the rates of
root and shoot respiration. Roots have been found to have
higher maintenance costs than shoots (Hansen and Jensen,
1977; Szaniawski, 1980; Johnson, 1990). These costs are
thought to be associated with active ion uptake by the roots
(Amthor, 1984). In only a few studies have di€erences in
respiration rate among above-ground tissues been quanti®ed
(Peterson and Zelitch, 1982; Ryan et al., 1995; Law et al.,
1999). Ryan et al. (1995) found very low rates of respiration
per unit of biomass in woody stems. Comparisons of
respiration rate among other above-ground tissues have
rarely been made within a single species (but see Peterson
# 2001 Annals of Botany Company
356
McCutchan and MonsonÐTissue-type, Development and Respiration
and Zelitch, 1982) despite the signi®cant proportion of total
biomass that structures other than leaves may comprise.
Respiratory ¯ux associated with growth and maintenance
will also vary with development. Respiratory costs associated with growth are important during biomass accumulation. As growth slows, respiratory costs associated with
tissue maintenance become proportionally more important
(McCree and Kresovich, 1978; Amthor, 1984). The developmental pattern of respiration has been studied in leaves
(Kidd et al., 1921; Azcon-Bieto et al., 1983a; Wen and
Liang, 1993; Radoglou and Teskey, 1997; Atkin et al., 2000;
Oleksyn et al., 2000), fruit (DeJong and Walton, 1989;
Walton et al., 1990), woody stems (Ryan, 1990), whole
shoots and roots (Szaniawski, 1980), and whole plants
(Farrar, 1980b). In all the tissues studied, respiration rates
are high in young tissues and decrease with maturity. Again,
in only a few studies has the developmental pattern of
respiration been measured in more than one tissue within a
single species (Peterson and Zelitch, 1982; Law et al., 1999).
Currently, we cannot make quantitative assessments of the
importance of various tissues or development on carbon
balance in native populations of plants, especially herbaceous perennials. In carbon balance models, growth respiration is estimated as a constant proportion of net primary
productivity (Agren et al., 1991; Raich et al., 1991),
although this relationship is likely to change when tissue
allocation patterns change, as occurs in response to
environmental variability (Walker et al., 1995; Hobbie and
Chapin, 1998) and as occurs seasonally in temperate plants.
The main goal of this study was to quantify seasonal
patterns of respiration in the above-ground tissues (leaves,
stems and reproductive structures) of two herbaceous
perennials, Bistorta bistortoides (Pursh) Small (Polygonaceae) and Campanula rotundifolia L. (Campanulaceae), in
their native habitats. These species were chosen because each
can be found in a variety of habitats, from montane to
tundra, which makes it possible to evaluate the e€ect of site
on development and tissue allocation. The species were also
part of a larger study in which respiration was quanti®ed
across both temporal and spatial gradients (Plumb, 1999). In
addition to the main goal stated above, comparisons were
made between biomass accumulation and respiration rate,
seasonal changes in the Q10 of respiration were measured,
and total tissue respiration (respiration per unit biomass tissue mass) was calculated at a single temperature
(15 8C) on each collection date to compare the magnitude of
respiratory loss among the above-ground tissues.
We hypothesized that respiration rate would decrease over
the growing season in each of these tissues and that the most
signi®cant decrease would occur before growth ceased.
Respiration rate and the seasonal pattern of respiration
should also vary signi®cantly among the three tissues. We
hypothesized that respiration rates would be highest in the
reproductive tissues, intermediate in the leaves, and lowest in
the stems. The di€erences would be associated with the cost
of building and maintaining these tissues. Reproductive
tissues grow throughout the season and can be made of
biosynthetically expensive compounds. Thus, respiration
rate should be high in reproductive structures throughout
the growing season. Leaves should have intermediate rates
because of the high cost of maintaining proteins associated
with photosynthesis. Stems should have the lowest respiration rates because they are biosynthetically cheap to build
and maintain.
M AT E R I A L S A ND M E T H O D S
Two herbaceous perennials, Bistorta bistortoides (Pursh)
Small (Polygonaceae) and Campanula rotundifolia L.
(Campanulaceae), were studied at three sites each in the
Rocky Mountains of Colorado (USA). B. bistortoides is a
common plant of arctic and alpine tundra and is also found
in both subalpine and montane meadows in Colorado.
Plants of B. bistortoides usually produce two to ®ve large
basal leaves and between zero and three in¯orescences per
year. C. rotundifolia exists over a much wider elevational
range. It can be found from the montane foothills of the
Rockies (1798 m) to the tundra fell®elds (3414 m). Plants of
C. rotundifolia tend to produce many stems which bear both
leaves and reproductive structures. Details of each of
collection site are given in Table 1.
T A B L E 1. Site name (as it appears in text), site elevation,
and length of growing season of the three Campanula
rotundifolia and three B. bistortoides sites studied
Elevation
(m)
Growing
season length
(d)
Species
Name
Bistorta bistortoides
Montane
Subalpine
Alpine
2710
3200
3410
78
78
79
Campanula rotundifolia
Foothill
Montane
Alpine
1800
2650
3410
120
99
73
The above-ground biomass of ®ve to eight plants was
collected before sunrise every 2 weeks from leaf emergence
to seed dispersal for each species at each site. One collection date was omitted at the alpine C. rotundifolia site. The
entire above-ground biomass of individuals of B. bistortoides
was collected; this consisted of two to four basal leaves and
one to two ¯ower stalks. Each in¯orescence consisted of
numerous small ¯owers. Three to ®ve shoots were collected
from individual C. rotundifolia plants. In C. rotundifolia,
only cauline leaves were measured because the few basal
leaves present had senesced by the ®rst collection date. Two
to six ¯owers, at various stages of development, were present
on each shoot. The above-ground biomass of individual
plants was brought back to the laboratory on ice where it
was divided into leaves, stems and reproductive tissues
( ¯owers, ripening ovaries, seeds). A portion of each tissue
was kept cold for respiration measurements while the rest of
the tissue was weighed to obtain the fresh biomass and then
dried at 55 8C for 3 to 7 d to obtain dry biomass. The tissues
were completely dry after 2 d.
Oxygen electrodes (Hansatech, King's Lynn, UK) were
used to measure dark respiration rate following the methods
McCutchan and MonsonÐTissue-type, Development and Respiration
Biomass (mg)
2000
1500
1000
500
0
2500
B
Biomass (mg)
2000
1500
1000
500
0
2500
C
2000
1500
1000
500
Seed
Dispersed
Mature
Seed
Young
Seed
0
Mature
Flowers
The initial growth phase was dicult to document in the
two species. Consequently, 30 to 60 % of the peak aboveground biomass had accumulated at the beginning of each
collection series. The pattern of above-ground biomass
accumulation varied among sites within each species (Figs 1
and 2). While the length of the growing season was similar
among the B. bistortoides sites (Table 1), peak biomass was
reached later in the growing season at the alpine and
subalpine sites than in the montane site (Fig. 1). In
C. rotundifolia, peak above-ground biomass occurred at
¯ower maturation in the alpine and foothill plants but at
seed maturation in the montane plants (Fig. 2). Stems of
the alpine B. bistortoides and C. rotundifolia grew throughout the season. C. rotundifolia leaves showed little increase
in biomass throughout the growing season. The plants from
both the B. bistortoides and C. rotundifolia montane sites
A
Young
Flowers
R E S U LT S
2500
Biomass (mg)
of Delieu and Walker (1981). The temperature of the
electrodes was maintained at 15 or 25 8C with circulating
water baths (Brinkman model RM6, Fisher Scienti®c Model
9105). Respiration rate was measured in air at 15 and 25 8C
in both B. bistortoides and C. rotundifolia. Plants were stored
at ‡8 8C until respiration rates were measured. Respiration
rate was found to be stable for at least 8 h after collection.
Rates were measured for 6 to 8 min after a stable respiration
rate was obtained. For each of the tissues, an attempt was
made to include material from the various age classes
represented within a single individual. For B. bistortoides, a
portion of each leaf was used for respiration measurements
and, for C. rotundifolia, several leaves along the length of
each stem were used. In both species, several pieces of stem
(approx. 2 cm long) were taken along the length of each
stem. Portions of the stem and leaf material were trimmed so
that they completely ®lled the area of the oxygen electrode
chamber. No relationship was found between the degree of
trimming and the respiration rate. Whole ¯owers of
C. rotundifolia were used for respiration measurements. If
the reproductive structures of C. rotundifolia were found in
multiple developmental stages on a single collection date,
then representatives of each stage were included in
the respiration measurements. The small ¯owers of
B. bistortoides were removed from the stem for respiration
measurements and approx. 50 ¯owers were placed in the
electrode chamber. Within B. bistortoides individuals, the
reproductive structures were developmentally similar. The
tissue samples were dried for 4 h at 100 8C and then stored
in a drying oven at 55 8C until dry biomass was measured.
Respiration rates were calculated on both a dry biomass
(nmol O2 s ÿ1 g ÿ1 d. wt) and above-ground tissue basis
(mmol O2 h ÿ1).
One-way ANOVAs were used to compare the change in
respiration rate over the growing season within each tissue
at each site. Two-way ANOVAs were used to compare
di€erences in respiration rates among the tissues at each site
and di€erences among the seasonal pattern of respiration
rate among the tissues at each site. All analyses were
performed using Microsoft Excel or JumpIn (SAS Institute
software).
357
Development
F I G . 1. Dry biomass (mg) accumulation over the growing season in
individuals of B. bistortoides from three sites in the Colorado Rockies:
(A) montane, (B) subalpine and (C) alpine. j, Reproductive structure
dry mass; , leaf dry mass; , stem dry mass. n ˆ 5±6 plants. Bars are
the s.e. for each tissue.
were considerably larger at peak biomass than those from
the other sites.
Respiration rate decreased signi®cantly over the growing
season in the three tissues of both species (P 5 0.0002)
except in the leaves of C. rotundifolia at 25 8C (Figs 3 and 4).
There was also signi®cant interaction between tissue type
358
McCutchan and MonsonÐTissue-type, Development and Respiration
400
A
Biomass (mg)
300
200
100
0
1
Biomass (mg)
400
2
4
5
6
7
B
300
200
100
0
400
1
2
3
4
5
6
7
C
Biomass (mg)
300
200
100
0
2
4
5
7
Development
F I G . 2. Dry biomass (mg) accumulation over the growing season in
Campanula rotundifolia shoots from three sites in the Colorado Rocky
Mountains: (A) foothill, (B) montane and (C) alpine. j, Reproductive
structure dry mass; , leaf dry mass; , stem dry mass. n ˆ 6±8
plants. Bars are the s.e. for each tissue. Codes for the developmental
stages are as follows: 1, young leaves; 2, small ¯ower buds; 3, large
¯ower buds; 4, mature ¯owers; 5, young seed; 6, mature seed; 7, seed
dispersed.
and the seasonal pattern of respiration (P 5 0.0001).
Generally, leaf respiration rate decreased less than that of
stems or reproductive structures during the growing season
and respiration rates of the reproductive structures remained
high throughout the growing season. The decrease in
respiration rate in the various tissues was not always large
or consistent. In some of the tissues, there was an increase in
rate between consecutive developmental stages. The pattern
and magnitude of the decrease in respiration rate over the
growing season was also dependent on the measurement
temperature. Despite signi®cant di€erences (P 5 0.05) in
the Q10 of respiration over the growing season, no consistent
pattern of change could be found (data not shown). Q10
values within each tissue appeared to ¯uctuate stochastically
during the growing season.
The respiration rate of B. bistortoides leaves decreased by
approx. 35 % when measured at 15 8C (Fig. 3). Most of the
decrease in rate occurred early in the growing season as
growth slowed. When measured at 25 8C, B. bistortoides
leaves in both the alpine and montane populations showed a
decrease in respiration rate from the ®rst to the last collection date, but there was occasionally an increase in respiration rate between collection dates ( for instance, between the
`young seed' and `mature seed' categories in the montane
leaves). Stems of B. bistortoides exhibited a relatively consistent decrease in respiration rate over the growing season
which was larger in magnitude (60±75 %) than that seen in
the leaves. The reproductive tissues of B. bistortoides had
developmental patterns that varied between sites and
temperatures. In the reproductive tissues of alpine and subalpine B. bistortoides, respiration rate generally dropped
sharply over the entire growing season. A similar pattern
was seen in the reproductive tissues of montane B. bistortoides when measured at 15 8C but, oddly, the rate measured
at 25 8C was very low on the ®rst collection date.
At all sites, C. rotundifolia leaves showed a very small
decrease in respiration over the season (approx. 25 % at
15 8C and 10 % at 25 8C) and there were intermittent
increases in rate throughout the season, especially in the
montane leaves (Fig. 4). C. rotundifolia stems, like those of
B. bistortoides, exhibited a larger drop in rate (31±74 %)
over the season, but also occasionally experienced increases
between collection dates. The reproductive tissues of alpine
and foothill C. rotundifolia maintained high respiration rates
until seed dispersal when respiration dropped by 80 to 90 %.
This decrease was more extreme when measured at 25 8C
than when measured at 15 8C. In the montane C. rotundifolia
reproductive tissues, respiration rate at 15 8C dropped at a
fairly constant rate throughout the season, but when
measured at 25 8C there was an initial rise in rate, maintenance of a high rate, and then a precipitous drop in rate.
Tissue type also had a signi®cant e€ect on respiration
rate (P 5 0.0001). In both species, the reproductive tissues
had signi®cantly higher respiration rates per unit biomass
than the leaves or stems (Figs 3 and 4). At seed maturation,
the respiration rate of the reproductive structures dropped
to values that were similar or lower than those of the leaf or
stem. Respiration rates of the C. rotundifolia reproductive
structures were more similar to leaf respiration rates at
15 8C than at 25 8C (Fig. 4). B. bistortoides leaves had
respiration rates that were intermediate between the rates of
the reproductive tissues and the stems (Fig. 3). The
respiration rate of the C. rotundifolia leaves was higher
than that of the stems at 15 8C (Fig. 4). At 25 8C, the leaf
rates were only slightly higher and, in some cases, similar to
those of the stems.
Total respiratory ¯ux (mmol O2 h ÿ1) for each of the
above-ground tissues was calculated on each collection date
McCutchan and MonsonÐTissue-type, Development and Respiration
A (15°C)
60
40
30
20
20
10
0
0
C (15°C)
80
D (25°C)
50
60
40
40
30
20
20
10
0
0
60
E (*15°C)
80
F (25°C)
50
60
40
40
30
20
20
10
Seed Dispersed
Mature Seed
Young Seed
Mature Seed
Young Seed
Mature Flowers
Young Flowers
Development
Mature Flowers
0
0
Young Flowers
Respiration Rate (nmol O2 s–1 g–1)
B (25°C)
40
60
Respiration Rate (nmol O2 s–1 g–1)
80
50
Seed Dispersed
Respiration Rate (nmol O2 s–1 g–1)
60
359
Development
F I G . 3. Seasonal patterns of respiration rate (nmol O2 s ÿ1 g ÿ1 dry mass) at 15 8C and 25 8C in leaves (ÐjÐ), stems (± ± ±d± ± ±), and
reproductive structures ( r ) of B. bistortoides from montane (A, B), subalpine (C, D), and alpine (E, F) sites. n ˆ 5±6 plants. Bars are the s.e.
for each tissue.
by multiplying the respiration rate at 15 8C by the dry
biomass of the tissue on the collection date. Total aboveground tissue respiration peaked at mid-season in montane
B. bistortoides but was fairly constant throughout the
growing season in the subalpine and alpine above-ground
biomass (Fig. 5). B. bistortoides leaves had a signi®cantly
higher total respiratory ¯ux than B. bistortoides stems and
reproductive tissues (Fig. 5). B. bistortoides stems and
reproductive structures had a similar respiratory ¯ux within
the alpine and subalpine populations. Peak above-ground
respiratory ¯ux varied with site in C. rotundifolia (Fig. 6).
Total above-ground respiratory oxygen uptake of
C. rotundifolia was highest early in the season at the
foothill site, at mid-season in the montane, and late in the
McCutchan and MonsonÐTissue-type, Development and Respiration
Respiration Rate (nmol O2 s–1 g–1)
360
50
40
40
30
30
20
20
10
10
Respiration Rate (nmol O2 s–1 g–1)
0
50
1
2
4
5
6
7
0
50
C (15°C)
40
40
30
30
20
20
10
10
0
Respiration Rate (nmol O2 s–1 g–1)
50
A (15°C)
50
1
2
3
4
5
6
7
0
50
E (15°C)
40
40
30
30
20
20
10
10
0
2
4
5
7
Development
0
B (25°C)
1
2
4
5
6
7
D (25°C)
1
2
3
4
5
6
7
F (25°C)
2
4
5
7
Development
F I G . 4. Seasonal patterns of respiration rate (nmol O2 s ÿ1 g ÿ1 dry mass) at 15 8C and 25 8C in leaves (ÐjÐ), stems (± ± ±d± ± ±), and
reproductive structures ( r ) of Campanula rotundifolia from foothill (A, B), montane (C, D), and alpine (E, F) sites. n ˆ 5±6 plants and bars
are the s.e. for each tissue. Codes for the developmental stages are as follows: 1, young leaves; 2, small ¯ower buds; 3, large ¯ower buds; 4, mature
¯owers; 5, young seed; 6, mature seed; 7, seed dispersed.
season in the alpine site. Respiratory ¯ux was similar in
C. rotundifolia leaves and stems within the foothill and
montane sites (Fig. 6). C. rotundifolia reproductive structures had the lowest total respiratory ¯ux of the three
above-ground tissues in all sites.
DISCUSSION
Respiration rate per unit biomass in Bistorta bistortoides
and Campanula rotundifolia leaves, stems and reproductive
structures decreased with tissue development (Figs 3 and 4).
A decrease in respiration rate with tissue age has also been
observed in leaves, cotyledons, fruits, whole shoots and
roots of other plants (Kidd et al., 1921; Farrar, 1980b;
Szaniawski, 1980; Azcon-Bieto et al., 1983; DeJong and
Walton, 1989; Walton et al., 1990; Wen and Liang, 1993).
Although respiration rate did decrease in all tissues over
the growing season, the decrease could rarely be ascribed to
a decrease in biomass accumulation. It is generally believed
McCutchan and MonsonÐTissue-type, Development and Respiration
A
Respiration Rate (µmol O2 h–1)
15
90
60
40
0
5
15
60
30
0
Respiration Rate (µmol O2 h–1)
10
1
B
90
120
A
0
Respiration Rate (µmol O2 h–1)
Respiration Rate (µmol O2 h–1)
120
4
5
6
7
B
12
9
6
3
1
15
90
60
30
Seed
Dispersed
Mature
Seed
Young
Seed
Mature
Flowers
0
Young
Flowers
2
0
C
Development
Respiration Rate (µmol O2 h–1)
Respiration Rate (µmol O2 h–1)
120
361
2
3
4
5
6
7
C
12
9
6
3
0
2
4
5
7
Development
F I G . 5. Total above-ground respiration rates (mmol O2
for
reproductive structures, leaves and stems of B. bistortoides from
montane (A), subalpine (B) and alpine (C) sites. j, Reproductive
structure respiration rate; , leaf respiration rate; , stem respiration
rate. The bar over each tissue rate represents s.e. n ˆ 5±6 plants.
F I G . 6. Total above-ground respiration rates (mmol O2 h ÿ1) for
reproductive structures, leaves and stems in Campanula rotundifolia
from foothill (A), montane (B) and alpine (C) sites. j, Reproductive
structure respiration rate; , leaf respiration rate; , stem respiration
rate. The bar over each tissue rate represents s.e. n ˆ 6±8 plants. Codes
for the developmental stages are as follows: 1, young leaves; 2, small
¯ower buds; 3, large ¯ower buds; 4, mature ¯owers; 5, young seed; 6,
mature seed; 7, seed dispersed.
that while biomass is accumulating, much of the respiratory
carbon ¯ux is associated with growth respiration (McCree
and Kresovich, 1978). In the species studied, only
B. bistortoides leaves and C. rotundifolia stems had
respiration rates that decreased as leaf and stem biomass
accumulation slowed (cf Figs 1 and 3 and Figs 2 and 4). In
both B. bistortoides stems and C. rotundifolia leaves,
respiration rate continued to decline after biomass
accumulation had ceased. In these tissues, it is possible
that maintenance costs decreased over the season.
h ÿ1)
362
McCutchan and MonsonÐTissue-type, Development and Respiration
Respiratory ¯ux associated with tissue maintenance has
been shown to decrease with tissue age (Merino et al., 1984)
and this decrease is correlated with a decrease in the
biosynthetic cost (i.e. proportional increase in structural
compounds with a concommitant decrease in lipids and
proteins) of the tissue (Penning de Vries et al., 1974;
Penning de Vries, 1975; Williams et al., 1987). It is not
known why tissue maintenance costs might decrease in the
leaves of one species but not in those of another. The
di€erences seen between the stems of the two species may be
related to di€erences in shoot morphology and stem
function. Stems of C. rotundifolia bear all of the photosynthetically active leaves (basal leaves had senesced early in
the growing season) and act as temporary storage sites for
carbohydrates (McCutchan, unpubl. res.). This may cause
C. rotundifolia stems to have high maintenance costs
throughout the growing season to accommodate carbohydrate transport and storage. In contrast, B. bistortoides
plants have large basal leaves and stems that do not appear
to store carbohydrates (McCutchan, unpubl. res.). In the
reproductive structures, high growth rates were not
associated with high respiration rates. In general, respiration rate dropped precipitously while ¯oral biomass
remained constant or increased slightly. In both species,
seed maturation is coincident with the lowest respiration
rate seen in the reproductive structures (Figs 3 and 4).
Respiration rate may not be associated with growth in the
reproductive structures of perennials for two reasons. First,
growth may continue throughout the season but be masked
by the senescence of some structures, such as the corolla
and sepals, while growth of others, such as pericarp and
ovules, continues. Second, large drops in respiration may
also be associated with decreases in maintenance respiration
as ¯oral structures are ®lled with storage compounds. It is
apparent from these results that the de®nition of general
functions that relate growth to respiration would have to be
modi®ed for di€erent tissues and species. Knowledge of
tissue construction costs or nitrogen content could improve
the accuracy of these relationships.
In addition to the lack of correlation seen between growth
and respiration, leaf respiration rates of both species often
exhibit apparently stochastic changes over the growing
season. This is especially true in leaves of C. rotundifolia
from the montane and foothill sites (Fig. 4). Night-time leaf
respiration rate is positively correlated with the previous
day's light intensity in a number of crop plants (Hansen and
Jensen, 1977; Azcon-Bieto and Osmond, 1983; Reddy et al.,
1991; Noguchi and Terashima, 1997; Atkin et al., 1998).
This relationship is thought to be mediated by the supply of
carbohydrates from the previous photosynthetic period
(Breeze and Elston, 1978; Azcon-Bieto and Osmond, 1983;
Mullen and Koller, 1988; Noguchi et al., 1996; Noguchi and
Terashima, 1997). The unusual variation seen in leaf
respiration rate may be caused by variability in the light
intensity on the day previous to the collection day. Low light
intensity on the previous day could result in lower
respiration rates on the collection day.
Very di€erent seasonal patterns of respiration were seen
when the whole tissue mass was considered. The total
respiratory ¯ux (oxygen uptake per hour) of the combined
above-ground tissues of individual plants either reached a
maximum at mid-season or was fairly constant until the end
of the growing season (Figs 5 and 6). That the total aboveground tissue respiration may remain constant throughout
a large portion of the growing season in these herbaceous
perennials is surprising because there is such a large change
in both biomass and respiration rate per unit biomass
during this period. On average, only 50 % of the aboveground biomass had accumulated in each population on the
®rst collection date and we might expect that the total
above-ground respiratory ¯ux would be low early in the
season. But, the large total respiratory ¯ux seen early in the
growing season was associated with high respiration rates
per gram of tissue. A similar phenomenon was seen when
total respiratory ¯ux of individual tissues was compared.
For instance, a tissue with a low metabolic activity (e.g.
stems) had a total respiratory ¯ux that was similar to that of
a tissue with higher metabolic activity (e.g. leaves or
reproductive structures) because stems were often larger
than leaves or ¯owers.
Di€erences among sites in biomass allocation and the
pattern of respiration with development resulted in variability in the pattern of total respiration in individual tissues
among the tissues, species and sites. For instance, carbon
¯ux from stems was considerably higher in individuals from
both species at the montane sites because of higher biomass
allocation to stems at these sites. The pattern of carbon ¯ux
from reproductive structures varied greatly among species
and sites. This was due to the greater proportion of aboveground biomass found in the reproductive structures of
B. bistortoides, variability in allocation to reproductive
structures among sites within a species, and also variability
in the developmental pattern of respiration per unit mass.
The documentation of these di€erences provides evidence
that models currently used to predict respiration in plant
tissues are too simplistic. In the species studied, it would be
impossible to predict respiration rate as a function of a single
variable, such as biomass, because respiration rate is a€ected
by tissue-type, development, and the interaction of these
variables. Species and site e€ects are also clearly important
in determining the developmental pattern of tissue respiratory ¯ux in B. bistortoides and C. rotundifolia. Environmental variables have been found to alter species
composition, phenology and ecosystem respiration in
tundra. Hobbie and Chapin (1998) found an increase in
ecosystem respiration and changes in species composition
and biomass allocation upon warming of small patches of
tundra. Year to year environmental variability was shown to
change patterns of phenology and biomass allocation in
tundra species (Walker et al., 1995). More empirical
evidence is needed to understand the e€ect of a series of
complex interactions between biotic and abiotic factors on
respiration in natural environments. While such studies have
been conducted in the last decade in a number of tree species
(McLaughlin et al., 1990; Amthor, 1991; Ryan et al., 1995,
1997; Pregitzer et al., 1998; Bolstad et al., 1999; Clinton and
Vose, 1999; Law et al., 1999; Atkin et al., 2000), they are still
lacking in shrubs, herbaceous perennials and annuals.
Many of the plant and ecosystem models that are used to
predict carbon balance have functions that are too simplistic
McCutchan and MonsonÐTissue-type, Development and Respiration
to describe accurately natural variation in plant respiration.
This study has provided evidence that respiration in native
perennial tissues cannot be de®ned with functions of growth
or biomass alone. Relationships between respiration and
growth and/or biomass are probably modi®ed by other
biotic and abiotic variables, including tissue construction
and maintenance costs, thermal environment, photosynthetically active radiation, and nutrient availability. The use of
a combination of several factors such as growth rate,
biomass, construction cost and nitrogen content, to predict
respiration within a tissue, might provide a more accurate
prediction of tissue respiration and ecosystem carbon ¯ux.
In addition, this study has emphasized the importance of
including all tissues in analyses of carbon balance because
small tissues (i.e. ¯owers) and tissues with low metabolic
rates (i.e. stems) may be responsible for up to 60 % of the
total respiratory carbon ¯ux from above-ground tissues.
AC K N OW L E D GE M E N T S
We thank William Adams III for the use of oxygen
electrodes and water baths, Amy Keller for her help in the
®eld, and Barbara Demmig-Adams, Steve Hand, Je€
Mitton and two anonymous reviewers for helpful comments on the manuscript. Logistical support was provided
by the NSF supported Niwot Ridge Long-Term Ecological
Research project and the University of Colorado Mountain
Research Station.
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