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Annals of Botany 87: 355±364, 2001 doi:10.1006/anbo.2000.1341, available online at http://www.idealibrary.com on Eects 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 eect of biomass accumulation on respiration rate and dierences in respiration rate among tissues were measured. Respiration rate diered 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 eux 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 aected 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 eect 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 dierences 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 eect 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 dierences 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 dicult 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 dierences in respiration rates among the tissues at each site and dierences 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 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 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 dierences (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 eect 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 s1 g1) B (25°C) 40 60 Respiration Rate (nmol O2 s1 g1) 80 50 Seed Dispersed Respiration Rate (nmol O2 s1 g1) 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 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 s1 g1) 360 50 40 40 30 30 20 20 10 10 Respiration Rate (nmol O2 s1 g1) 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 s1 g1) 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 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 h1) 15 90 60 40 0 5 15 60 30 0 Respiration Rate (µmol O2 h1) 10 1 B 90 120 A 0 Respiration Rate (µmol O2 h1) Respiration Rate (µmol O2 h1) 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 h1) Respiration Rate (µmol O2 h1) 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 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 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 dierences seen between the stems of the two species may be related to dierences 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 dierent 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 dierent 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. Dierences 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 dierences 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 aected by tissue-type, development, and the interaction of these variables. Species and site eects 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 eect 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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