Elevated carbon dioxide and temperature effects on rice yield, leaf ...

Paddy Water Environ (2015) 13:313–324 DOI 10.1007/s10333-014-0447-x

ARTICLE

Elevated carbon dioxide and temperature effects on rice yield, leaf greenness, and phenological stages duration Nuno Figueiredo • Corina Carranca • Henrique Trindade • Jose´ Pereira Piebiep Goufo • Joaõ Coutinho • Paula Marques • Rosa Maricato • Amarilis de Varennes

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Received: 30 January 2014 / Revised: 11 May 2014 / Accepted: 23 May 2014 / Published online: 11 June 2014 Ó The International Society of Paddy and Water Environment Engineering and Springer Japan 2014

Abstract The present field experiment was conducted during two consecutive cropping seasons in central Portugal to study the effects of simultaneous elevation of carbon dioxide concentration ([CO2]) (550 lmol mol-1) and air temperature (?2–3 °C) on japonica rice (Oryza sativa L. ‘‘Ariete’’) yield, crop duration, and SPAD-values across the seasons compared with the open-field condition. Open-top chambers were used in the field to assess the effect of elevated air temperature alone or the combined effect of elevated air temperature and atmospheric [CO2]. Open-field condition was assessed with randomized plots under ambient air temperature and actual atmospheric [CO2] (average 382 lmol mol-1). Results obtained showed that the rice ‘‘Ariete’’ had a moderate high yielding under openfield condition, but was susceptible to air temperature rise of ?2–3 °C under controlled conditions resulting in reduction of grain yield. The combined increase of atmospheric [CO2]

with elevated air temperature compensated for the negative effect of temperature rise alone and crop yield was higher than in the open-field. SPAD-readings at reproductive stage explained by more than 60 % variation the straw dry matter, but this finding requires further studies for consolidation. It can be concluded that potential increase in air temperature may limit rice yield in the near future under Mediterranean areas where climate change scenario poses a serious threat, but long term field experiments are required.

N. Figueiredo C. Carranca (&) R. Maricato Instituto Nacional de Investigaçaõ Agra´ria e Veterina´ria, Quinta do Marqueˆs, Av. Repu´blica, Nova Oeiras, 2784-505 Oeiras, Portugal e-mail: [email protected]; [email protected]

J. Pereira Polytechnic Institute of Viseu, IPV, Agricultural Polytechnic School of Viseu, ESAV, Quinta da Alagoa, 3500-606 Viseu, Portugal

C. Carranca A. de Varennes Biosystems Engineering Center (CEER) ISA/UL, Lisbon, Portugal C. Carranca lnstituto de Cieˆncias Agra´rias e Ambientais Mediterraˆnicas (ICAAM), Univ. E´vora, Nućleo da Mitra, Apartado, 947002 E´vora, Portugal

Keywords Maturation duration Modeling Open-field Open-top chamber SPAD-reading

Introduction Rice (Oryza sativa L.) is one of the most important food crops in the world and a staple for more than half of the

J. Coutinho Chemistry Centre, University of Tra´s-os-Montes and Alto Douro, UTAD, Quinta de Prados, 5000-801 Vila Real, Portugal P. Marques Centro Operativo e Tecnolo´gico do Arroz, Salvaterra de Magos, Portugal

H. Trindade J. Pereira P. Goufo Centre for the Research and Technology of Agro-Environmental and Biological Sciences, CITAB, University of Tra´s-os-Montes and Alto Douro, UTAD, Quinta de Prados, 5000-801 Vila Real, Portugal

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global population. It has a wide physiological adaptability and is grown successfully in tropical, subtropical, and temperate regions. The optimum temperature for maximum rice photosynthesis is 25–30 °C for daytime maxima and 20 °C for the nighttime maxima (Sreenivasan 1985; IRRI (Int. Rice Res. Inst.) 1997). Higher yields are obtained in temperate countries than in tropical areas; the average yield of paddy rice in European countries is 5 t ha-1 and that of Asia 4 t ha-1, but the maximum potential yield of modern varieties is 13 t ha-1 in tropics and 15 t ha-1 in temperate regions (Tran 1997; Biswas and Ntanos 2002). Rice productivity does not only vary amongst countries but also within the same country based on the different agro-ecological zones and the production system used (Biswas and Ntanos 2002). The European Union (EU) has a production of rough rice of 3 million tons per year and ranks 17th (0.5 %) among main world producers, whereas it ranks only 19th in terms of consumption (3.5 million tons per year). In Europe, more than 140 rice cultivars have been produced in France, Spain, Italy, Greece, and Portugal (Confalonieri and Bocchi 2005). In the EU, Portugal is the first per capita consumer of rice and the fourth producer (6 t ha-1, 28,000 ha) contributing to 5.3 % of the total European production (Figueiredo et al. 2013). Rice varieties mainly produced in Europe are japonica and indica. The first generally refers to some traditional varieties selected before the 2nd World War, but also to some varieties selected between the 1970s and the 1990s (semidwarf) and high yielding. These varieties require lower temperature for ripening than indica varieties (Krishnan et al. 2011). Crop duration is an important trait in rice and other cereals, in particular because it correlates positively with yield potential (De Raı¨ssac et al. 2004). The growth duration of a rice crop varies from 3 to 8 months depending on the cultivar and environmental conditions. Most japonica type varieties are medium and mediumlate cultivars (cycle longer than 150 days) with only few early varieties (Krishnan et al. 2011). Akita (1989) observed in IRRI rice varieties an increasing yield when crop duration increased from 95 to 110 days, with a maximum constant yield of 9 t ha-1 when the season was longer than 110 days. In rice, most differences among short-, medium- and late-term varieties are due to the duration of the vegetative phase (De Raı¨ssac et al. 2004). Variations in environmental factors can have influence on the duration of this phase, even when expressed in thermal time; sensitivity to photoperiod is one classical example. Atmospheric carbon dioxide (CO2) is a substrate for plant photosynthesis. The effect of rising atmospheric CO2 concentration [CO2] on photosynthesis and productivity is reported to be more pronounced in C3 plants such as rice

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(Wassmann et al. 2009). High [CO2] reduces the stomata conductance, resulting in reduced transpiration, and increased net primary production (Haque et al. 2006; Ainsworth 2008; Cheng et al. 2009). IPCC (2007) estimated that atmospheric [CO2] has risen from approximately 280 lmol mol-1 in pre-industrial times to 380 lmol mol-1, and will reach 550 lmol mol-1 by 2,050. In the absence of strict control of emissions, the atmospheric [CO2] is likely to reach 730–1,020 lmol mol-1 by 2,100. Since CO2 and other greenhouse gases (GHGs) alter physical radiation properties and the energy balance of the atmosphere, they influence the global temperature regime. Therefore, simultaneously with the increase in the concentration of GHGs, the global average air temperature is projected to increase between 1.8 and 4.0 °C by the end of the present century relative to the mean value for 1980–1999. The increase in atmospheric [CO2] and projections of further increases in global air temperature stimulated studies on the effects of climatic variables on important food crops. These are particularly relevant for Mediterranean areas where climate change has been projected with extreme events (Figueiredo et al. 2013). To date, most studies have focused only on rice responses to CO2 enrichment photosynthesis, water relations, phenology, organ formation, dry matter (DM) production and distribution, carbon (C) and nitrogen (N) metabolism, as well as grain yield and its components (Wang et al. 2011). The ability of rice plants to tolerate higher temperatures depends on different thermo tolerance mechanisms at biochemical and metabolic levels, membrane stability, synthesis of heat shock proteins, and photosynthetic activities (Krishnan et al. 2011). Mohammed and Tarpley (2009) and Madan et al. (2012) reported that both high day and high night temperatures have negative effects on rice spikelet fertility and yields. High day temperatures beyond a critical threshold during sensitive development stages like gametogenesis and flowering lead to low seed-set. Mohammed and Tarpley (2009) attributed the year-to-year variation in rice grain yield and quality to the nighttime temperature increase during the critical stages of development. Although elevated [CO2] per se increases productivity of C3 crops such as rice, the increasing frequency and intensity of short-duration high temperature events ([33 °C) may pose a serious threat to agricultural production (Madan et al. 2012). Most research on the individual effects of CO2 and temperature alone effects have been restricted to crop yield and phenological parameters of plants grown in controlled environments. Data on interactive effects of CO2 and temperature rise under field conditions are rare. The proper use of N fertilizers can also markedly increase rice yield and improve quality. Crop N is closely associated with leaf chlorophyll, since a great amount of


leaf N is contained in chlorophyll molecules. Leaf N is related with grain yield in rice (Esfahani et al. 2008). Nitrogen contributes to carbohydrate accumulation in culms and leaf sheaths during the pre-heading stage and in the grain during the ripening stage (Swain and Sandip 2010; Goufo et al. 2014a). Leaf N concentration is thus a sensitive indicator for the dynamic changes in plant N, and N monitoring during the growth period is essential to achieve an efficient N fertilizer management and higher grain yield. Readings of cereal leaves using a chlorophyll-meter reading may provide information about the plant N status. The Soil Plant Analysis Development (SPAD) meter is an example of a simple, rapid, non-destructive, and portable diagnostic tool to measure the greenness or relative chlorophyll content of leaves (Gholizadeh et al. 2009; Neto et al. 2011). For a particular plant species, a higher SPADvalue usually indicates a healthier plant. SPAD-values are thus appropriate to predict whether response to additional topdress N is expected (Piekielek et al. 2008). Little information on SPAD-values for rice across the season is available, in particular in response to environmental stresses. The succession of rice development stages (phenology) depends on air and floodwater temperature and on photoperiod (day-length) (Krishnan et al. 2011). The different phenological events differ in their sensitivity to high temperature, depending on plant species and genotype. When rice is exposed to high temperatures during the vegetative stage, individual plant height, tiller number, and DM may be considerably reduced (Krishnan et al. 2011). Rice can grow with daytime temperatures as high as 40 °C during the vegetative stage, whereas floral development is very sensitive to high temperatures. Therefore, temperature may affect the growth duration of the rice crop to a great extent. Only one reference (Bhattacharyya et al. 2013) was found to report the effects of the interaction between temperature and CO2 elevation on phenological stages, but no results were given for the effects on crop duration. In the present study, a japonica rice variety (Oryza sativa L. cv. Ariete) was grown in open-field under natural sunlight, temperature and [CO2], but also in open-top chambers (OTCs) to increase the temperature (by the OTC effect) and the [CO2]. Rice management in the OTCs was the same and simultaneous with the open-field cultivation. Therefore, the overall objectives of this work were to assess the simultaneous effects of elevated [CO2] ? temperature and temperature per se in controlled environments, in comparison with the natural ambient open-field condition on i) rice yield and crop duration, ii) leaf greenness across the season, and iii) SPAD-values at specific phenological stage in order to predict the crop yield.

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Materials and methods Field experiment A field experiment with japonica rice variety (Oryza sativa L. cv. Ariete) was conducted for two consecutive seasons (2011 and 2012) at Salvaterra de Magos (Tagus Valley, central Portugal; latitude: 39°2.20150 N, longitude: 8°44.2570 W, elevation: 18 m above sea level). This area is the main region for rice production in Portugal. The experimental design consisted of three treatments arranged in a randomized complete block design and three replicates, in a total of nine blocks (Fig. 1a). Each block was 4.0 m 9 4.0 m, 4.0 m apart from each other. Treatments were as follows: elevated [CO2] ? temperature, elevated temperature (OTC effect), and the unchambered (openfield) control plots (around 375 lmol CO2 mol-1 air). To change the climatic variables, six large open-top chambers (OTC = 4 m wide 9 3 m height 9 2 m open-top diameter, 30 tilt), covered with a polyethylene film (1-mm thickness and 75 % light transmittance, provided by EstufasMinho, S.A., Faõ, Portugal) (Fig. 1b), were placed on a previous prepared (chisel and laser) lowland for paddy conditions: three OTCs were for elevated [CO2] ? temperature and three for the temperature rise (OTC effect). Details on the construction and operation of OTCs have been provided by Pereira et al. (2013). In the three OTCs for CO2 enrichment, a system using pure industrial CO2 injection was installed to fumigate CO2 during the daynight time (24 h per day). It operated from May to October 2011 and 2012 in order to have a concentration of 550 lmol CO2 mol-1, which represented the expected [CO2] range by the middle of the 21st century (IPCC 2007; Goufo et al. 2014b). Several sensors connected to a datalogger (DL2, Delta-T Devices, Cambridge, UK) were installed inside each OTC (Fig. 1c) and outside the chamber to monitor the climatic parameters: for [CO2], a probe (GMP222, Vaisalia, Finland) was used; and for temperature and humidity, a sensor (RHT2y, Delta-T Devices, Cambridge, UK) was used. The air in each OTC was circulated by two fans (EDM-100 °C 12 V, Soler & Palau Ltd, Portugal). The CO2 fumigation system operated in on–off mode control with a continuous sampling of CO2 level. When CO2 injection was necessary, the data-logger acted over an electronic valve (7321B 12 V, Parker Hannitin SpA, Gessate, Italy) linked to a pure industrial CO2 tank through a high-density polyethylene tube. Inside each elevated-[CO2] OTC, the CO2 distribution tube had several emission holes and was located around the sidewalls and kept at the crop canopy level throughout the season. Carbon dioxide concentration was continuously monitored with an infrared gas transmitter (GMP111, Vaisalia, Finland) linked to a real-time data acquisition and

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Fig. 1 A partial aspect of experimental site (a) installed in a rice field at Salvaterra de Magos (central Portugal); an aspect of the octagonal chamber with OTC (b); internal probes for CO2 (left, down) and air

temperature and humidity (right), a fan for air circulation (left, top), and a closed PCV chamber for measurement of GHG emissions inside the OTC (c)

a control system to maintain the concentration around the target level. All data were collected and/or controlled with a sampling interval of 30 s and storage time of 10 min (Pereira et al. 2013; Goufo et al. 2014d). Rice ‘Ariete’ was direct seeded in the open-field and OTCs on 27 May, 2011 and 23 May, 2012 at a rate of 200 kg (dry seeds) ha-1 and cultivated under intermittent water logging regime. In the OTC-treatments, rice was cultivated as in the open-field, but was maintained at the enriched [CO2] (552 ± 98.4 and 547 ± 73.0 lmol CO2 mol-1 air, respectively, in 2011 and 2012) and at the ambient [CO2] (388 ± 27.2 and 375 ± 46.0 lmol CO2 mol-1 air, respectively, in 2011 and 2012). Temperature was elevated in the six OTCs by the OTC effect (Fig. 2a, b). The Anthropic soil (IUSS Working Group 2006) was representative for rice production in Portugal. It had a clay texture (17, 28 and 55 % of sand, silt and clay, respectively) in the 0–60-cm layer. In the surface (0–20-cm

layer), the bulk density was 1.1 g cm-3, the pH(H2O)was 5.9, the cationic exchange capacity was 22.7 cmol(?) kg-1, and the content of organic C and total N was 24 and 2.4 g1 kg-1, respectively. Methods used for the evaluation of the physic-chemical characteristics of the soil are those routinely used in the Instituto Nacional de Investigaçaõ Agra´ria e Veterina´ria. All the experimental plots received the same rates and types of fertilizers. A NP mineral fertilizer (20–20–0) was mechanically broadcast at a depth of 20 cm in May as a basal dressing preceding crop seeding at a rate of 60 kg NH4N ha-1, and a sulfamid (40 % N) was manually applied on the floodwater at a rate of 60 kg N ha-1 as topdressing at tillering, in July. No potassium was added to the soil in both years as the soil was rich, whereas 60 kg ha-1 of phosphorus (P) was incorporated into the soil as part of the basal dressing in both seasons. After rice seeding, the water regime was intermittent, i.e., flooding—midseason drainage (for plant

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Fig. 2 Seasonal daily air temperature (maximum, average, minimum) in the open-field (O–F) and inside the chambers OTC during the rice growth in 2011 (a) and 2012 (b); mean monthly temperature and accumulated rainfall during the growth seasons in 2011 and 2012 (c)

rooting, about 1 week after rice germination, and twice for weed control during a few days at the tillering)—reflooding—drainage (3 weeks before crop harvest) (Fig. 3). Floodwater height varied from 5 to 20 cm depending on plant growth, in the open-field as well as the OTCs, as it passed through holes located at the bottom of the polyethylene film surrounding the OTCs. Irrigation water had an average pH 8.0, electric conductivity of 0.7 dS m-1, low levels of mineral N, high level of chloride content (71 mg Cl- l-1), 30–48 mg Ca2? l-1, 51–87 mg Na? l-1, and 7–10 mg K? l-1. ‘‘Ariete’’ is a cultivar moderately sensitive

to salinity and should not be negatively affected by salts present in the water. The experiments were kept free from weeds using herbicides. The cultural practices used in the experiment for the two consecutive seasons were similar to the typical agricultural management used by Portuguese rice farmers for the last 14 years and have been thoroughly described by Goufo et al. (2014c). The climate of the region is Mediterranean-type. In the open-field, daily meteorological data (rainfall, maximum, minimum, and mean air temperature, solar radiation and wind speed) were collected with an automatic weather

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Fig. 3 Cultural practices and date of sampling in seasonal rice ‘Ariete’ growths (2011 and 2012), at Salvaterra de Magos (central Portugal) (Pereira et al. 2013)

station placed near the site of the study. Mean ambient air temperature during both growth cycles (2011 and 2012) varied from 18 to 19 °C in May to 20–21 °C in August (Fig. 2c). In both seasons in general, maximum air temperature did not go over 34 °C (Fig. 2a, b). Minimum rainfall occurred in June–July (\10 mm) and the maximum in October (90–100 mm) for both years (Fig. 2c). The wind speed in 2011 and 2012 ranged from 3.8 to 8.1 m s-1. Global solar radiation did not vary in the two seasons and averaged 5,787 W m-2. Inside the OTCs, the mean temperature was ?2 ± 1.1 °C and ?3 ± 1.8 °C above the open-field, respectively, in 2011 and 2012. In summer 2012, a higher number of days greater than 34 °C inside the OTCs, including above 38 °C was registered compared with the open-field this year and with the OTCs in 2011(Fig. 2a, b). Across both seasons, SPAD-502 (Minolta, Japan) readings were recorded in the afternoon (15–16 h) at different phenological stages (4th leaf, tillering, internode elongation, flowering, grain fill, and maturity) (Fig. 3) in each plot using the youngest fully expanded Y-leaf of rice plants (Dobermann and Fairhurst 2000), also known as flag leaf in the reproductive stage. One reading corresponded to the average of ten measurements. At harvest (19 October 2011 and 10 October 2012), corresponding to 149 and 140 days after sowing (DAS), all plants were removed from the center of plots (corresponding to an average of 175 plants ha-1). Plant material was separated into straw and grain, dried (65 °C for 48 h) and weighed to estimate yield (kg DM ha-1). Statistical analysis Analysis of variance (ANOVA) was performed by the General Linear Model using the STATISTICA 6.0

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software to evaluate effects of years, treatments [openfield, and elevated [CO2] ? temperature and temperature (OTC effect)], and growth phases (DAS) on DM yield and SPAD-values. Means separation was determined for significant differences by the Bonferroni’s test, at P \ 0.05. Polynomial equations were established for SPAD-values across seasons (P \ 0.05) depending on the treatment. Linear regression equations to predict crop yield were fitted for significant (P \ 0.05) overall SPADvalues for both seasons at specific phenologic stage and treatment.

Results Crop productivity Years (2011 and 2012) and treatments (open-field, temperature and [CO2] ? temperature elevation) significantly affected yield (Table 1). A higher grain yield (11 t ha-1) was observed in 2011 (Fig. 4) due to increased [CO2] (552 ± 98 lmol mol-1 air), higher than the yield (7 t ha-1) obtained in plants grown in the open-field this year (388 ± 27 lmol CO2 mol-1 air). The lowest yield (5 t ha-1) was measured in 2012 in the OTCs for [CO2] ? temperature elevation (Fig. 4). This year, the maximum temperature in summer (August and September) was above 34 °C (Fig. 2b) and caused a 29 % decrease in weight compared with the average grain yield in the openfield for both seasons (7 t ha-1), where the maximum daily temperature was always below 34 °C (Fig. 2a, b). As to straw DM yield, no significant differences were observed between treatments in 2011 and in the open-field in 2012 (6 t ha-1), but straw DM was reduced 50 % due to the


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Table 1 ANOVA results for DM yield of japonica rice ‘Ariete’ cultivated in clay loam soil at Salvaterra de Magos (central Portugal) for two continuous seasons (2001 and 2012)

Table 2 ANOVA for SPAD-values in leaves of japonica rice ‘Ariete’ cultivated in clay loam soil at Salvaterra de Magos (central Portugal)

ANOVA

P

ANOVA

F value

F value

P

3.9

*

Year (Y)

86.4

***

Year (Y)

Treatment (T)

11.6

***

Treatment (T)

184.1

***

Plant organ (P) Y9T

41.8 31.6

*** ***

Time of sampling (S) Y9T

202.1 43.3

*** ***

Y9P

–

***

ns

Y9S

15.9

T9P

5.0

*

T9S

10.8

***

Y9T9P

6.0

**

Y9T9S

4.1

***

Year = 2011, 2012; treatment = open-field (control), and temperature and CO2 ? temperature elevation; plant organ = straw, grain; P Probability value, ns Data not shown, *, **, *** F-values nonsignificant (P C 0.05), and significant for P \ 0.05, P \ 0.01, and P \ 0.001, respectively according to the Bonferroni’s test

Year = 2011, 2012; Treatments = open-field (control), and temperature and CO2 ? temperature elevation; time of sampling = days after sowing (DAS); P Probability value, *, *** F-values significant for P \ 0.05 and P \ 0.001, respectively according to the Bonferroni’s test

increase in temperature by the OTC effect (Fig. 2b) in 2012 (3 t ha-1) (Fig. 4).

the OTCs (SPAD = 42), where SPAD-values did not differ from each other. Changes in the relative amount of chlorophyll over time, measured indirectly by the SPAD technique were also observed (Table 2; Fig. 5A). Greater SPAD-values were observed at the flowering phase (68-77 DAS) for all treatments in response to topdressing at tillering and the rise of temperature and [CO2] ? temperature (SPAD = 49). Under the open-field, SPAD-values differed in both seasons, with lower values in 2012. Lower SPADvalues in 2012 in the open-field were probably a consequence of a lower ambient [CO2] (\350 lmol mol-1 of air) from middle July till middle September and/or simultaneous higher maximum daily temperatures ([34 °C) during this period. In 2011, the ambient [CO2] was

Leaf greenness and duration of phenological stages Years (2011 and 2012), treatments (open-field, temperature and [CO2] ? temperature elevation) and dates of sampling (DAS) significantly affected leaf greenness given by SPAD-values taken in the youngest fully expanded Y-leaf across both seasons (Table 2). In general, the interaction of tested factors also affected the SPAD-readings. The overall SPAD-value in 2011 (41) was significantly higher than in 2012 (SPAD = 40). Considering the mean effect of years and sampling dates, a significantly lower SPAD-value was measured in the open-field (SPAD = 37) compared with

Year 2011

Year 2012

16000

Dry matter (kg DM ha-1)

14000 12000 10000 8000 6000 4000 2000 0 Open-field

CO 2+Temperature

Straw

Temperature

Open-field

CO 2+Temperature

Temperature

Grain

Fig. 4 DM yield by rice ‘Ariete’ cultivated in clay loam soil at Salvaterra de Magos (central Portugal) in response to the interaction effect of years and treatments (open-field, and temperature and CO2 ? temperature elevation). (n = 36; vertical bars denote 0.95 confidence intervals)

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A

SPAD-value

Open-field

CO 2+Temperature

Temperature

54 52 50 48 46 44 42 40 38 36 34 32 30 28 26 24 22 20 53

58

66

73

87

108

121

53

58

66

73

87

DAS

DAS

Year 2011

Year 2012

108

121

B b 50 47 SPAD = 16 + 0.629x-0.0042x2, x=DAS 44 n=8; R²= 0.75; P