Influence of temperature and soil drying on respiration of individual roots in citrus: integrating greenhouse observations into a predictive model for the field

In citrus, the majority of fine roots are distributed near the soil surface – a region where conditions are frequently dry and temperatures fluctuate considerably. To develop a better understanding of the relationship between changes in soil conditions and a plant’s below-ground respiratory costs, the effects of temperature and soil drying on citrus root respiration were quantified in controlled greenhouse experiments. Chambers designed for measuring the respiration of individual roots were used. Under moist soil conditions, root respiration in citrus increased exponentially with changes in soil temperature ( Q 10 = 1·8–2·0), provided that the changes in temperature were short-term. However, when temperatures were held constant, root respiration did not increase exponentially with increasing temperatures. Instead, the roots acclimated to controlled temperatures above 23 ∞ C, thereby reducing their metabolism in warmer soils. Under drying soil conditions, root respiration decreased gradually beginning at 6% soil water content and reached a minimum at <2% soil water content in sandy soil. A model was constructed from greenhouse data to predict diurnal patterns of fine root respiration based on temperature and soil water content. The model was then validated in the field using data obtained by CO 2 trapping on root systems of mature citrus trees. The trees were grown at a site where the soil temperature and water content were manipulated. Respiration predicted by the model was in general agreement with observed rates, which indicates the model may be used to estimate entire root system respiration for citrus. Key-words : Root distribution; simulation; soil water content; temperature. INTRODUCTION In both natural and agricultural systems, root respiration represents a substantial cost to the overall carbon economy of a plant. Lambers, Atkin & Scheurwater (1996a) estimate that roots consume 8–52% of the carbon fixed daily during photosynthesis to supply energy for new root construction, ion uptake and maintenance. Respiratory energy is also required to support associations with symbiotic organisms such as mycorrhizal fungi (Peng et al . 1993; Nielsen et al . 1998) and nitrogen-fixing bacteria (Ryle et al . 1984), as well as for defence against fungal pathogens (Singh & Singh 1971; Uritani & Asahi 1980). A variety of factors influence the rate at which carbon is consumed during respiration, including differences among species (Poorter et al . 1991; Lambers et al . 1996a), plant age (Poorter & Pothmann 1992), and growth conditions (Greenway & West 1973; Farrar 1981; Lambers, Stulen & van der Werf 1996b; Zog et al . 1996). However, in wellaerated, mature field systems, the effects of soil moisture and temperature typically dominate (e.g. Maier & Kress 2000). Other factors such as mean root age, nutrient availability (unless amended with fertilizer), and microbial associations remain relatively constant over time (Marschner 1995; Smith & Read 1997). Their effects on root respiration are usually undetectable during shortor long-term measurements. Consequently, moisture and temperature are often considered the main driving variables used to model root respiration (e.g. Carlyle & Ba Than 1988; Alm & Nobel 1991; Burton et al . 1998). Such models can explain a significant portion of the observed variation in CO 2 evolution from soils and roots. Ordinarily, plant respiration increases exponentially as a function of temperature under normal growing conditions (Salisbury & Ross 1996). Based on this observation, the effects of temperature on root respiration would be easily defined for a particular species. This also suggests that respiratory costs would be higher in warmer soils. However, root respiration has been shown to acclimate to contrasting temperatures in certain species, including six grass (Smakman & Hofstra 1982; Fitter et al . 1998; Gunn & Farrar 1999) and five boreal tree (Tjoelker, Oleksyn & Reich 1999) species. When acclimation occurs, temperature-based predictions of respiration become more difficult. The relationship 782 D. R. Bryla et al. © 2001 Blackwell Science Ltd, Plant, Cell and Environment , 24 , 781–790 between temperature and respiration is further complicated when soil moisture conditions are also considered because respiration typically declines as soil water is depleted (Palta & Nobel 1989a, 1989b; Burton et al . 1998). Consequently, existing respiration models may be inappropriate under certain conditions for many species. The purpose of this study was to develop a model for estimating root respiration of mature citrus trees. An earlier study showed that respiration by citrus roots acclimates to warm soil temperatures and slows during drought (Bryla, Bouma & Eissenstat 1997). The model in the current study was based on data collected in the greenhouse, and included terms for temperature, temperature acclimation, and soil moisture. To characterize root respiratory responses to changes in soil conditions, small chambers designed for measuring individual root branches in situ were used. These chambers enabled us to manipulate only a portion of the root system without affecting the entire physiology of the tree. The model was validated using data collected in the field on full-grown trees. MATERIALS AND METHODS Soil conditions and fine root distribution in the field Fine root length density (<2 mm in diameter) was determined at various soil depths on 20-year-old ‘Valencia’ orange [ Citrus sinensis (L.) Osbeck] trees grown in a rootstock trial located 7 km south-east of Avon Park, FL, USA. Soil at the site is a deep, uniform, Astatula fine sand (Typic quartzipsamment) with low cation-exchange capacity, low organic matter (<1%), low water-holding capacity, and essentially no horizontal development or soil structure. Trees were budded to six different rootstocks, planted 4·6 m apart within rows and 6·2 m apart between rows, and arranged in a completely randomized block design in groups of three trees per block. The rootstocks were: Carrizo citrange (CC) [ C. sinensis (L.) Osb. ¥ Poncirus trifoliate (L.) Raf.]; Cleopatra mandarin (CM) ( Citrus reticulata L.); Swingle citrumelo (SC) ( Citrus paradisi Macf. ¥ P. trifoliate ); sour orange (SO) ( Citrus aurantium L.); trifoliate orange (TO) ( P. trifoliate ); and Volkamer lemon (VL) ( Citrus volkameriana Tan. & Pasq.). The ranking of rootstocks based on the size of canopy volume at 10 years of age was VL a CM a CC > SO >> SC > TO. The ranking based on root fineness or specific root length [cm root g 1 dry weight (DW)] was TO >> VL > CC > SC > CM a SO (Graham & Syvertsen 1985; Eissenstat 1991). Soil temperature and water potentials were monitored continuously during 1994 and 1995 under six trees on sour orange rootstock. Soil temperature was measured using copper–constantan thermocouples buried 5 cm deep, and soil water potentials were measured using calibrated WaterMark soil moisture sensors (Ben Meadows Company, Inc., Atlanta, GA, USA) buried 15 and 40 cm deep. The thermocouples and moisture sensors were located 1 m from the base of the trees and read hourly using a datalogger (Model 21X; Campbell Scientific Inc., Logan, UT, USA). In mid-March 1995, soil cores (5 cm diameter) were collected from beneath the canopy of 48 trees (six rootstocks ¥ eight replicates) in 0–10 cm, 10–20 cm, 20–30 cm, 30–60 cm and 60–100 cm depth increments. To eliminate any overlap between rootstocks, cores were collected from the middle tree in each block. A second set of cores was also collected from the top 10 cm of soil beneath each tree and divided into depth increments of 2 cm. Each core was taken 1 m from the base of the trees and stored at 5 ∞ C before processing. Roots were washed from the soil cores, stained with neutral red to enhance their contrast, and imaged using a flatbed scanner (HP ScanJet II; Hewlett Packard, Palo Alto, CA, USA). Root lengths were measured from the scanned images using image-analysis software (Delta-T SCAN; Delta-T Devices Ltd, Cambridge, UK), and divided by the soil volume to calculate root length density. Single root respiration in the greenhouse The response of root respiration to changes in soil conditions was measured on 2-year-old sour orange trees located in a ventilated glasshouse at the Pennsylvania State University in Centre County, PA, USA. Trees were grown in 20 dm 3 pots filled with Candler fine sandy soil (Typic quartzipsamment with 0·1% organic matter) collected from the Citrus Research and Education Centre in Lake Alfred, FL, USA. Respiration experiments were limited to only one rootstock because a considerable amount of labour and resources was required for these experiments. Data collected in the greenhouse experiments described below were used to develop a model for estimating respiration in the field. Chamber for measuring single root respiration A chamber was designed to measure respiration of a single branch of fine roots growing in soil (Fig. 1). The chamber bottom was constructed from a 10 cm polyvinyl chloride (PVC) plastic tube (5 cm inner diameter), cut in half and glued to a PVC frame (11·5 cm ¥ 8·5 cm ¥ 0·5 cm). Plastic plates were glued to the ends of the half tube to create a compartment for soil. Small brass fittings were threaded into the end plates to attach flexible Bev-A-Line ® (Thermoplastic Processes, Inc., Stirling, NJ, USA) tubing for air inlet and outlet. A U-shaped, stainless steel tube (0·8 cm outer diameter) was inserted inside the chamber to circulate water from a heated/refrigerated water bath to control chamber temperature. The chamber lid was made from clear Plexiglas ® (Rohn & Haas Co., Philadelphia, PA, USA) (8·5 cm ¥ 11·5 cm ¥ 0·5 cm), and provided a means to monitor root growth after a chamber was installed. All plastic was covered with clear Teflon ® (E.I. Dupont de Nemours & Co., Wilmington, DE, USA) tape to prevent the chamber from absorbing CO 2 during measurements. Some 3 mm foam (H-O Products, Winsted, CT, USA) was used to provide an airtight seal between the chamber