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1 August 2004 Out of Sight, Out of Mind: Thermal Acclimation of Root Respiration in Arctic Ranunculus
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Abstract

Respiration rates, thermal sensitivity, and thermal acclimation potential of root respiration were investigated in Ranunculus from the Arctic. Comparisons of three species (R. glacialis, R. nivalis and R. acris subsp. pumilus) used plants grown on a mountain or in a glasshouse for 6 wk at contrasting soil temperatures (5.4 and 14.5°C, respectively). Northern and southern ecotypes of two species of Ranunculus (R. pygmaeus, and R. acris subsp. acris), together ranging from Svalbard (79 °N) to Scotland (56°N), were similarly compared after 2 wk in a growth cabinet at 5 and 15°C. Respiration rates varied at standard measurement temperatures; R. nivalis and R. pygmaeus grown on the mountain or at 5°C had the highest respiration, followed by other alpine snowbed species (R. glacialis and R. acris subsp. pumilus) and R. acris subsp. acris from the arctic lowland; R. acris subsp. acris from Scotland had lowest rates. Respiration was temperature sensitive for all populations, increasing progressively between 5 and 20°C (Q10 (5–15): 1.2–2.4).

Extent and type of acclimation of root respiration varied with no clear latitudinal pattern emerging. Acclimation to a 10°C increase in growth temperature was achieved through: change in temperature sensitivity (shown by changes in Q10 (5–15) values) (R. acris subsp. pumilus); or reduction in absolute rates (R. pygmaeus from Svalbard, R. acris subsp. pumilus and R. nivalis). Complete acclimation occurred in R. acris subsp. pumilus and R. pygmaeus, whereas R. acris subsp. acris from Scotland and R. glacialis did not acclimate. Plants that adjust root respiration (e.g., R. pygmaeus from Svalbard and R. acris subsp. pumilus) to maintain a positive carbon balance, may tolerate predicted temperature increases in arctic regions. Plants with high rates of root respiration and/ or high sensitivity to temperature as well as poor acclimation potential, (e.g., R. glacialis) may only persist in cold microhabitats.

Introduction

Root respiration is an important but often overlooked component of plant performance. The balance between rates of photoassimilate production by green tissue and their use in respiration determines a plant's capacity to survive and grow. Root and rhizome respiration accounts for 10 to 66% of the carbon fixed daily by a plant (Lambers, 1989; van der Werf et al., 1994), and up to 60% of total soil respiration (Bowden et al., 1993). Northern or alpine plant species or ecotypes often have higher root respiration rates than their southern or lowland counterparts (Higgins and Spomer, 1976; Crawford and Palin, 1981; Sowell and Spomer, 1986; Graves and Taylor, 1988), particularly at cooler growth temperatures. Respiration is generally more temperature sensitive than photosynthesis, meaning that increased temperatures brought about by global climate change (IPCC 2001), may result in the respiration of a significantly higher proportion of the carbon fixed by photosynthesis (Woodwell, 1990; Loveys et al., 2002). In arctic plants, root respiration is of major importance because of the large proportion of biomass allocated belowground (Wielgolaski, 1972; Shaver and Chapin, 1991), high respiration rates and high temperature sensitivity. The risk of a negative carbon balance with increased growth temperature in these plants may be reduced if they are able to thermally acclimate, by reducing either their absolute rates of root respiration or the thermal sensitivity of respiration.

Despite the importance of root respiration, few studies document its response to increased growth temperatures; particularly so for arctic plants. Some species adjust to increased growth temperatures by reducing root respiration rates by up to 40% (Higgins and Spomer, 1976; Abebe, 1990; Tjoelker et al., 1999; Atkin et al., 2000a; Atkin and Tjoelker, 2003). This is achieved through changing the proportions of control exerted by adenylates, substrates, and enzyme capacity on respiratory flux (Covey-Crump et al., 2002). The extent to which plants reduce their absolute respiration rates and thermal sensitivity of respiration varies greatly between species, with no clear pattern yet emerging (Atkin and Tjoelker, 2003).

This study investigated respiration rates, thermal sensitivity, and the potential for thermal acclimation of root respiration to experimental warming for plants from a range of sites—from High Arctic to temperate latitudes and upland to lowland altitudes. Three arctic Ranunculus species (R. glacialis, R. nivalis and R. acris subsp. pumilus) grown on a mountain or in a glasshouse for 6 wk at contrasting soil temperatures (5.4 and 14.5°C, respectively) were compared. Northern and southern ecotypes of two species of Ranunculus (R. pygmaeus (from Svalbard and Sweden) and R. acris subsp. acris (from Sweden and Scotland)) were similarly compared after 2 wk in a growth cabinet at 5 and 15°C. Acclimation is defined as the adjustment of root respiration rate to compensate for a change in growth temperature. Plants may acclimate their respiration rates partially or fully, with full acclimation providing homeostasis (Atkin et al., 2000b), i.e. identical respiration rates in plants grown and measured at contrasting temperatures. Acclimation ability is indicated by the long-term ratio (LTR10 (5–15)) (Larigauderie and Körner, 1995), i.e. the ratio of respiration rate of the plants grown and measured at 15 and at 5°C, with a value of 1.0 showing complete acclimation. Acclimation can occur by reductions in thermal sensitivity of root respiration at increased growth temperature, as measured by Q10 (5–15) values (“Type I” acclimation, Atkin and Tjoelker, 2003); and reductions in absolute rate of respiration (“Type II” acclimation, Atkin and Tjoelker, 2003). Q10 was calculated at 5 and 15°C since this investigation concerns respiration at soil temperatures experienced by plants in the Arctic. Thus, the complementary field and laboratory experiments in the present study evaluate the acclimation potential in arctic, temperate, alpine, and lowland species of the same genus.

Methods

SPECIES AND SITES

The genus Ranunculus includes species with contrasting latitudinal ranges within Europe, from High Arctic to temperate ecosystems. Study species were herbaceous perennials with small rhizomes and nonmycorhizal roots (Harley and Harley, 1987; Cooper, 1996). They were R. acris subsp. acris L., R. acris subsp. pumilus (Wahlenb.) Á. and D. Löve, R. glacialis L., R. nivalis L., and R. pygmaeus Wahlenb; nomenclature follows Tutin et al. (1993). Ranunculus acris occurs in wet meadows and habitats (Harper, 1957); R. nivalis is found in wet meadows, along the edges of mountain streams, on tundra, and in snowbeds (Polunin, 1959); R. pygmaeus grows in snowbeds to at least 2000 m a.s.l. (Hultén, 1968) and in moist places on tundra (Polunin, 1959). Ranunculus glacialis is characteristic of wet snowbeds with stony ground and sparse vegetation (Gjærevoll, 1956; Gjærevoll and Bringer, 1965) and is the species found at the highest altitudes in the European Alps (up to 4275 m a.s.l., Crawford, 1989).

Plant material was collected from sites at three latitudes comprising a gradient from upland temperate, through lowland and upland subarctic, through to High Arctic (Table 1). In Svalbard the R. pygmaeus site lay 1.5 km northwest of Ny-Ålesund, in a late melting snowbed on a well drained southwest-facing moraine at 25 m a.s.l. In northern Sweden, R. pygmaeus, R. nivalis, and R. glacialis were collected on Slåttajåkka mountain (1190 m a.s.l.) from late-melting snowbeds that were constantly damp and cold, while R. acris subsp. pumilus was collected on the same mountain (at 830 m a.s.l.) in an area snow covered in June but with drier soils by the end of summer. Ranunculus acris subsp. acris was collected just outside the Abisko Research Station (380 m a.s.l.), Sweden, and a Scottish population of R. acris subsp. acris was collected from a wet meadow community on a west-facing slope above Drumochter Pass (500 m a.s.l.).

FIELD EXPERIMENT

Individually potted plants from Slåttajåkka (R. nivalis, R. glacialis and R. acris subsp. pumilus) were grown on the mountain at 1000 m a.s.l., or under natural lighting in a glasshouse at Abisko Research Station. Mean soil and air temperatures were 5.4 ± 1.9°C and 6.3 ± 3.2°C (mountain) and 14.5 ± 2.9°C and 14.7 ± 3.3°C (glasshouse). Pots in the glasshouse were watered regularly and 100 ml of nutrient solution containing 19.5 mg N, 3 mg P, and 14.1 mg K applied weekly. Root respiration rates for six randomly selected plants of each species were determined after 6 wk at 5 and 15°C, using an infrared gas analyzer (IRGA, model LCA3, ADC, Herts., UK) and a leaf chamber with water jacket. The same roots were used at both temperatures and stored in air-saturated water between measurements. The aboveground tissues experienced a photosynthetic photon flux density (PPFD) of 500 μmol·m−2·s−1 throughout. Root mass was oven dried at 60°C and weighed for calculation of respiration rate.

GROWTH CABINET EXPERIMENT

Ranunculus pygmaeus from Svalbard and Slåttajåkka, and R. acris subsp. acris from Abisko and Scotland, were grown in a glasshouse at Bradford University, UK. Nonflowering plants of equivalent sizes were cleaned of soil and grown in full strength Rorison's solution (Gigon and Rorison, 1972) in a Birchover growth cabinet with continuous light (PPFD of 400 μmol·m−2·s−1), mimicking the arctic growing season. Relative humidity (RH) was 50 to 70%. Plants were kept at a constant 5 or 15°C for 2 wk, and then the roots of six intact plants from each population were measured at 5, 10, 15, and 20°C using an IRGA. The same plants were measured at all temperatures and aboveground tissues received PPFD of 400 μmol·m−2·s−1 throughout. Respiration rate was measured on four successive days using temperature order 15, 5, 20, 10°C and plants were returned to their growth conditions between measurements. Roots were dried at 60°C and weighed.

STATISTICAL ANALYSES

Data were analyzed using the “R” statistical package ( http://www.r-project.org/). Respiration rates in the field experiment were analyzed by a two-way ANOVA with interactions on all data (variables: species, treatment, measurement temperature) and for each species separately (variables: treatment, measurement temperature). Growth cabinet experiment data was analyzed by repeated-measures ANOVA with interactions on all data (variables: species, ecotype, treatment, measurement temperature) and individually for each ecotype (variables: treatment, measurement temperature). The Welch two-sample t-test was used for treatment effects on Q10 (5–15), and to test for homeostasis of root respiration.

Results

ABSOLUTE RATES OF ROOT RESPIRATION

Root respiration rates are summarized in Figures 1 and 2. Absolute respiration rates varied between species (species effect; field experiment: F (2,60) = 57.78, P < 0.001; growth cabinet experiment: F(1,40) = 24.56, P < 0.001), and between northern and southern ecotypes of R. pygmaeus but not R. acris subsp. acris (growth cabinet: species*ecotype interaction, F(1,40) = 15.19, P < 0.001). Ranunculus nivalis and R. pygmaeus grown on the mountain or at 5°C had the highest respiration, followed by other snowbed species (R. glacialis and R. acris subsp. pumilus) and R. acris subsp. acris from Abisko; R. acris subsp. acris from Scotland had lowest rates. Respiration rates of plants grown at 5°C were higher for the High Arctic population of R. pygmaeus than the alpine subarctic population (ecotype effect at 5°C growth, growth cabinet: F(1,10) = 13.95, P = 0.004).

TEMPERATURE SENSITIVITY OF RESPIRATION

Root respiration rates increased with measurement temperature (field: F(1,60) =184.23, P < 0.001; growth cabinet: F(3,120) =132.42, P < 0.001). For example, rates for R. pygmaeus from Svalbard grown at 5°C increased from 14.8 to 32.9 nmol CO2 g−1 s−1 between 5 and 20°C. The mean Q10 (5–15) values for the mountain and 5°C grown plants (Table 2) were 1.2 to 2.4; those of glasshouse and 15°C grown plants ranged from 1.5 to 2.2.

ACCLIMATION

The extent and type of acclimation to a 10°C increase in growth temperature varied, with no clear latitudinal pattern emerging. Type I acclimation (change in temperature sensitivity shown by changes in Q10 (5–15) values): only R. acris subsp. pumilus differed significantly in Q10 (5–15) between mountain (1.2) and glasshouse (2.2) grown plants (t = 2.46, df = 6.39, P = 0.047). Type II acclimation (reduction in absolute rates): root respiration of glasshouse and 15°C grown plants were lower than for those of corresponding cooler growth conditions (treatment effects, field: F(1,60) =16.47, P < 0.001; growth cabinet: F(1,40) = 22.41, P < 0.001). For example, at 15°C, Svalbard R. pygmaeus grown at 15°C respired 14.3 nmol CO2 g−1 s−1, compared to 25.5 nmol CO2 g−1 s−1 for plants grown at 5°C. Significantly lower respiration rates at the warmer growth treatment occurred for Svalbard R. pygmaeus (F (1,10) = 15.47, P = 0.003) in the growth cabinet and R. acris subsp. pumilus and R. nivalis (F (1,20) =16.52, P < 0.001 and F (1,20) = 4.80, P = 0.040, respectively) in the field experiment.

Homeostasis was measured in R. acris subsp. pumilus and both ecotypes of R. pygmaeus (Table 3). LTR10 (5–15) s indicate that complete acclimation occurred in R. acris subsp. pumilus and in Svalbard R. pygmaeus; partial acclimation in R. acris subsp. acris from Abisko and in R. pygmaeus from Slåttajåkka, whereas R. acris subsp. acris from Scotland and R. glacialis did not acclimate.

Discussion

Respiration rates of plants grown experimentally on the mountain and in the growth cabinet at 5°C were similar to those of undisturbed arctic Ranunculus in the field (Cooper, 1996). High rates of root respiration, especially in cold soils emerging from snow at the beginning of the growth season, enable rapid growth of leaves for effective use of diurnal sunlight for photosynthesis. No clear latitudinal pattern emerged in response of root respiration to growth temperature. The ecotype acclimating most to a 10°C increase in growth temperature was R. pygmaeus from Svalbard; its site was poorly vegetated and supported thin dark soil that dried out following snowmelt, warmed quickly and subsequently followed air temperature. In contrast, the Slåttajåkka snowbed had higher vegetation cover, was continually fed by melting snow and thus the soil remained damp and cold all summer. An insulating vegetation layer buffers arctic soil temperature against the warming effect of the sun and reduces melting of permafrost (Coulson et al., 1993; van der Wal and Brooker, 2004). Dry soils also warm faster than wet soils (Coulson et al., 1993). The Svalbard site therefore, may have been warmer during part of the growing season with larger diurnal temperature amplitude than the snowbed site on top of Slåttajåkka. Differential moisture content and thermal stability of the sites of origin may explain the differences in acclimation potential between R. pygmaeus from Svalbard and Slåttajåkka. Likewise, R. acris subsp. pumilus, originating from a site susceptible to summer drying and warming, thermally acclimated to warmer growth temperatures, in contrast with R. glacialis, originating from a damper and colder site.

It appears that there are two strategies for arctic and arctic-alpine plants: (i) plants with limited or no potential for acclimation of root respiration are restricted to damp, cold, relatively thermally stable soil environments; (ii) plants able to thermally acclimate by reducing the rates or temperature sensitivity of root respiration can survive in widely fluctuating or warmer soils. Plants that can thermally acclimate (e.g., R. pygmaeus from Svalbard and R. acris subsp. pumilus from Slåttajåkka) may survive increases in summer temperature, whereas those unable to do so (e.g., R. glacialis) may only survive if their belowground habitats remain cold. High rates and temperature sensitivities of root respiration, coupled with limited ability to thermally acclimate their root respiration rates may explain the decline or disappearance of typical snowbed species from central Norway and Finnish Lapland (Virtanen et al., 2003). They may also account for the recent rise in the lower altitudinal limit for R. glacialis and other snowbed species in the European Alps and the Jotenheimen mountains, Norway (Grabherr et al., 1994, 1995; Klanderud and Birks, 2003).

Acknowledgments

This research was financed by the Natural Environmental Research Council, under the Arctic Terrestrial Ecology Special Topic Programme (grant number GST/02/530). The author thanks: A. D. Headley for assistance during the project; C. O'Hare for help in the field; staff of Abisko Scientific Research Station for hospitality during field work; and J. A. Baddeley, S. J. Coulson, I. D. Hodkinson, G. Søvik, and two anonymous reviewers for comments on an earlier manuscript.

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Appendices

FIGURE 1.

Belowground respiration rates (mean ± SE, n = 6) (nmol CO2 gdry wt−1 s−1) at 5 and 15°C for arctic-alpine Ranunculus species grown on Slåttajåkka and in a glasshouse at Abisko, Sweden. The dotted line shown for R. acris subsp. pumilus represents homeostasis. Significant differences in rates between mountain and glasshouse grown plants are indicated by *P < 0.05, ** P < 0.01

i1523-0430-36-3-308-f01.gif

FIGURE 2.

Belowground respiration rates (mean ± SE, n = 6) (nmol CO2 gdry wt−1 s−1) of R. pygmaeus from Svalbard and Slåttajåkka (Sweden), and R. acris from Abisko (Sweden) and Scotland grown in a growth cabinet at 5 or 15°C, and measured at 5 to 20°C. Dotted lines shown for both R. pygmaeus populations represent homeostasis. Significant differences in rates between the plants grown at 5 and 15 °C are indicated by ** P < 0.01

i1523-0430-36-3-308-f02.gif

Table 1

Details of study sites. Dates and sources of the data are as follows: Svalbard: 1969–1992, Norwegian Meteorological Offcie, 1985; Sweden: 1961–1990 ANS records; Scotland: 1931–1960 British Meteorological Office. Mean soil temperature and daily amplitude of soil (6 cm depth) and air (5 cm) are shown for a warm 5-d period during July (GRANT Squirrel data logger). Ranunculus species used in a)field experiment, b)growth cabinet experiment

i1523-0430-36-3-308-t01.gif

Table 2

Q10(5–15)s for root respiration. ‘Q10(5–15) cool': plants grown on Slåttajåkka mountain, Sweden, and in a growth cabinet at 5 °C. ‘Q10(5–15) warm': plants grown in a glasshouse in Abisko, Sweden) and in a growth cabinet at 15 °C. Significant difference indicated by * (P < 0.05). Where no significant difference exists, the average Q10(5–15) value is shown

i1523-0430-36-3-308-t02.gif

Table 3

Tests for homeostasis and mean long term respiration ratios (LTR10(5–15)) (± SE, n = 6) for root respiration of plants grown on Slåttjåkka, (Sweden) and measured at 5°C compared with those grown in the glasshouse at Abisko (Sweden) and measured at 15°C. Likewise plants grown and measured at 5°C in a growth cabinet are compared with plants grown and measured at 15°C. T-test (t) results are indicated as follows: *** P < 0.001, ** P < 0.01, * P < 0.05, ns = not significant (= complete acclimation). An LTR Value of 1.0 indicates complete acclimation; as the value increases, the acclimation ability decreases

i1523-0430-36-3-308-t03.gif
Elisabeth J. Cooper "Out of Sight, Out of Mind: Thermal Acclimation of Root Respiration in Arctic Ranunculus," Arctic, Antarctic, and Alpine Research 36(3), 308-313, (1 August 2004). https://doi.org/10.1657/1523-0430(2004)036[0308:OOSOOM]2.0.CO;2
Published: 1 August 2004
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