Genotypic Differences in Water Use Efficiency of Common Bean under ...

Genotypic Differences in Water Use Efficiency of Common Bean under Drought Stress Agronomic Application of Genetic Resources

V. H. Ramirez Builes, T. G. Porch,* and E. W. Harmsen ABSTRACT

Common bean (Phaseolus vulgaris L.) is extensively grown in production zones where water is limiting. Crop water use efficiency is the ratio of biomass or seed yield produced per unit of water evapotranspired in a particular environment. Transpiration efficiency (TE) is the ratio of yield per unit of water transpired. The objectives of this study were to: (i) determine the water use efficiency (WUE) for six common bean genotypes (BAT 477, Morales, SEN 3, SEN 21, SER 16, and SER 21) in the greenhouse and for two genotypes in the field (Morales and SER 16) and (ii) determine TE for two common bean genotypes using estimated evapotranspiration rates in the field. Three greenhouse trials and two field trials were conducted during 3 yr in Puerto Rico. Three water levels in the greenhouse and two in the field were applied. Actual evapotranspiration was estimated using the generalized Penman–Monteith model based on aerodynamic and surface resistance, and with drainage type lysimeters in the field. Differences among genotypes for WUE were found in the greenhouse experiments, with SEN 3 and SER 21 showing superior WUE in several treatments. In the field, TE and WUE were affected by water level, and TE was consistent with previously reported coefficients for common bean.

C

ommon bean is the most important food legume (Broughton et al., 2003) and is an important source of calories, protein, dietary fiber, and minerals (Singh et al., 1999). In addition, common bean provides an essential source of protein for more than 300 million people worldwide (Beebe and McClafferty, 2006). Annual production of dry and snap bean exceeds 21 million Mg and represents more than half of the world’s total food legume production (Miklas et al., 2006). Drought is the major constraint to common bean production, resulting in significant yield reductions in 60% of global bean production areas (White and Singh, 1991). In addition, competition among crops for production area in certain regions has resulted in a shift of dry bean production to more marginal zones associated with increased abiotic stresses (Porch et al., 2007), such as drought and heat. The extent and duration of both intermittent and terminal drought stress in common bean are directly associated with the reduction in yield (Singh, 1995). Drought effects are amplified by interactions with other sources of stress, such as disease, insect pressure, high temperature, and low soil fertility. Developmentally, root growth and development (Kuruvadi and Aguilera 1990; Sponchiado et al., 1989), dry matter accumulation (Boutraa and Sanders, 2001), and reproductive development (e.g., Beebe et al., 2011; Calvache et al., 1997; Muñoz-Perea et al., 2007; Norman et al., 1995, p. 208–224) are particularly affected by V.H. Ramirez Builes, Centro Nacional de Investigaciones de Café, Manizales, Colombia; T.G. Porch, USDA-ARS, Tropical Agriculture Research Station, Mayagüez, PR 00680; and E.W. Harmsen, Dep. of Agricultural and Biosystems Engineering, Univ. of Puerto Rico, Mayagüez, PR 00681. Received 3 Sept. 2010. Corresponding author ([email protected]). Published in Agron. J. 103:1206–1215 (2011) Posted online 26 May 2011 doi:10.2134/agronj2010.0370 Copyright © 2011 by the American Society of Agronomy, 5585 Guilford Road, Madison, WI 53711. All rights reserved. No part of this periodical may be reproduced or transmitted in any form or by any means, electronic or mechanical, including photocopying, recording, or any information storage and retrieval system, without permission in writing from the publisher.

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drought stress, while drought can result in differential effects at different developmental stages (Debaeke and Aboudrare, 2004; Kramer and Boyer, 1995; Laffray and Louguet, 1990; Nielsen and Nelson, 1998: Ramirez-Vallejo and Kelly, 1998; Terán and Singh, 2002). Although the specific mechanisms of drought tolerance have not been elucidated, associations with abscisic acid synthesis (Lizana et al., 2006), stomatal control (Laffray and Louguet, 1990), transpiration rate (Ritchie, 1983), and relative water content (Stayanov, 2005) have been reported. Due to the lack of methods for measuring and selecting for plant response to drought that directly result in heritable yield improvement, and due to the complex genetic control of drought tolerance, genetic improvement of common bean for drought has been slow. Thus, effective approaches for the evaluation of drought are needed to help mitigate the effects of decreasing water availability. Robust drought tolerance is conferred by traits that result in stable yield in the presence of water stress, as opposed to mechanisms of escape, such as early maturity. The evaluation and selection for drought tolerance should therefore be focused on the selection of traits that directly affect yield under stress conditions. Water use efficiency is a measure of water used per unit of yield. An economic yield model for drought evaluation was developed by Passioura (1977), where grain yield = water use × WUE × harvest index [HI]), and where WUE is the ratio of biomass or seed yield produced per unit of water evaporated and transpired and HI is the ratio of grain yield to total biomass yield. Thus, in this approach, traits are selected that: (i) affect plant response to drought during an extended period of plant development, (ii) influence global plant growth and development, and (iii) apply to the specific target environment (Condon et al., 2004). Therefore, improvement of WUE or HI can result in grain yield improvement. These traits are interdependent, Abbreviations: DP, deep percolation below the root zone; ETc, crop evapotranspiration; GPM, generalized Penman–Monteith; HI, harvest index; LAI, leaf area index; RO, surface runoff; TE, transpiration efficiency; WUE, water use efficiency.

A g ro n o my J o u r n a l • Vo l u m e 10 3 , I s s u e 4 • 2 011

Table 1. Climatic conditions and the drought intensity index (DII) for the greenhouse (Mayaguez, Puerto Rico) and field (Juana Diaz, Puerto Rico) experiments during 2005, 2006, and 2007. Variable (average of daily values) Location Average daily temperature, ºC) Mean max. daily temperature, ºC Mean min. daily temperature, ºC Relative humidity, % Vapor pressure deficit, kPa Solar radiation, MJ m–2 d–1 Wind speed, m s–1 DII‡

2005 July–Sept.

2006 July–Sept.

2006 Oct.–Dec.

2006 Feb.–Apr.

2007 Jan.–Apr.

greenhouse 27.6 –† – 84.3 – – – 0.47

greenhouse 26.9 33.9 22.6 78.8 0.76 5.0 0 0.63

greenhouse 26.6 31.3 21.8 77.4 0.94 5.3 0 0.48

field 24.6 29.9 19.4 70.8 0.89 19.3 2.7 0.31

field 24.7 30.0 20.6 64.4 1.1 17.3 2.9 0.72

† Not determined. ‡ DII = 1 – (trial average yield under drought stress/yield under nonstress or reduced-stress condition).

however, and thus yield compensation must be considered when selecting for one or more of these characteristics. In common bean, variation in WUE has been found among cultivars (Ehleringer et al., 1990; Ehleringer and Osmond, 1991) and has been used for the evaluation of germplasm under water-limiting conditions (e.g., Foster et al., 1995; Pimentel et al., 1999). Pimentel et al. (1999) recommended the use of intrinsic WUE, the photosynthetic rate for a given stomatal conductance, for selection of efficient genotypes at the flowering stage of development. Carbon isotope discrimination was also proposed as an indirect measure of yield under drought due to its association with WUE and yield in bean (Ehleringer et al., 1990; White et al., 1990; Zacharisen et al., 1999). While little investigation on TE has been completed, a study using weighing lysimeters determined the mean TE coefficient for common bean in the semiarid tropics of South Africa to be 3.26 ± 0.25 g kPa kg–1 (Ogindo and Walker, 2004). The TE was defined by the Bierhuizen and Slatyer method (Tanner and Sinclair, 1983), which is the crop aboveground (aerial) biomass (dry matter [DM] of stems, leaves, and fruit) divided by the mass of water transpired during the accumulation of that biomass (T), and is represented by

TE =

DM k = T VPD

[1]

Equation [1] indicates that the correlation between DM and T is dependent on k, which is a species-dependent water-use constant, and the atmospheric vapor pressure deficit (VPD), which defines the drying capacity of the air or the driving force for evaporation and transpiration. The mechanisms behind variability in TE in common bean are unknown, but heliotropic leaf movement has been associated with TE (Ehleringer and Osmond, 1991). Due to the importance of the consideration of both transpiration alone and evapotranspiration when calculating WUE, both WUE and TE were estimated in this study. The objectives of this study were to: (i) estimate the WUE for six common bean genotypes under greenhouse and field environments, and (ii) determine the TE and k constant for two common bean genotypes using estimated evapotranspiration rates in the field. MATERIALS AND METHODS Greenhouse Experiments to Study Water Use Efficiency The greenhouse experiments were performed at the USDAARS Tropical Agricultural Research Station in Mayagüez,

Puerto Rico (18º12´22˝ N, 67º8´20˝ W, 18 m above sea level) to study WUE. Three trials were conducted, including one during July to September 2005, the second during July to September 2006, and the third during October to December 2006, and meteorological data were recorded in the center of the greenhouse at plant height (Table 1). In 2005, four common bean genotypes were evaluated, the cultivar Morales (Beaver and Miklas, 1999), and three germplasm lines BAT 477, SER 16, and SER 21 (all developed at CIAT in Colombia). During 2006, SEN 3 and SEN 21 (also from CIAT) were added to the four genotypes evaluated in 2005. Seed of Morales was provided by James Beaver (University of Puerto Rico, Mayaguez), and seed of the germplasm lines developed for drought tolerance, BAT 477, SEN 3, SEN 21, SER 16, and SER 21, were provided by Steve Beebe (CIAT, Colombia). BAT 477 is small cream, SEN 3 and SEN 21 are small black, and SER 16 and SER 21 are small red common bean seed types. All genotypes tested have a type II plant habit, except for BAT 477, which has a type III plant habit. Three seeds of each genotype were planted per pot (15.5-cm diameter by 11-cm depth) with Sunshine mix no. 1 (Sun Gro Horticulture, Vancouver, BC, Canada) and Osmocote fertilizer (14–14–14 [N–P2O5–K 2O], Scotts Miracle-Gro Co., Marysville, OH) and were thinned to one plant per pot at the first trifoliolate stage. Similar studies using small pots for abiotic stress experiments have been performed under greenhouse conditions and have been effective at identifying genotypic differences (Markhart, 1985; Porch, 2006). Substrate field capacity (SFC), the maximum water retention capacity for the substrate, was measured after saturating, covering, and draining the substrate of 12 pots for 7, 24, and 48 h. The SFC was assumed to be the maximum water retention capacity. Volumetric moisture content was measured with a theta probe soil moisture sensor (ML2X, Delta-T Devices, Cambridge, UK), and the SFC was determined to be 0.53 (±0.010) m3 m–3. Three water levels were used: the nonstress treatment, where 80% of the SFC was applied; the Stress Level 1 treatment, where 50% of the SFC was applied before flowering and 60% of the SFC was applied after flowering; and the Stress Level 2 treatment, where 20% of the SFC was applied before flowering and 40% of the SFC was applied after flowering. The treatments were started after the full expansion of the second trifoliolate. The plants were watered every morning, and the volumetric moisture content (θv) was measured at specific developmental phases. Daily watering was required because the water retention capacity of

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the pots was low and the plants used all of the available water in the 1-d period. Based on the substrate water retention capacity, we determined the appropriate amount of daily water application as described above. At no time during the experiments was soil moisture depleted to the terminal drought stress level. The WUE in the greenhouse trials was estimated as the ratio of seed yield per plant divided by the total volume of water applied. The sample unit for these trials was a single plant, while the experimental unit was the average of two plants. The three water treatment levels were replicated four times, and the experiment was planted in three separate trials as indicated above. The experiment was analyzed as a split-plot experimental design. The main plot was the water level, and the sub-plot was the genotype.

each irrigation event, every 3 or 4 d. Two flow meters were placed in the irrigation supply lines, one on the reduced stress and the second on the drought stress treatment supply line. In 2006, 18% less water was applied to the stress plot (388 mm) than to the reduced stress treatment (472 mm). In 2007, 33% less water was applied to the stress plot (313 mm) than to the reduced stress treatment (467 mm). Agronomic practices related to crop management were consistent during the whole experiment. The field plot was treated with pre-emergent herbicide, fertilized with 10–10–10 (N–P–K) with micronutrients at a rate of 400 kg ha–1, mechanically and hand cultivated during crop growth, and treated with pesticides as needed to control insect pests.

Field Experiments to Study Water Use Efficiency and Transpiration Efficiency

Actual crop evapotranspiration (ETc) was measured using two methods. The water balance method used 12 drainage-type lysimeters installed in the field in 2005. Drainage lysimeters have been used successfully in previous evapotranspiration studies (e.g., Boman, 1991; Karam et al., 2005; Pereira and Adaixo, 1991) and can provide satisfactory estimates of water use during 3- to 4-d intervals (Caspari et al., 1993). Using the lysimeters, ETc was calculated as ETc = P + I – RO – DP + (ΔS), where P is precipitation, I is irrigation, RO is surface runoff, DP is deep percolation below the root zone, and ΔS is the change in root zone moisture storage (all units are in millimeters). The lysimeters were composed of round polyethylene containers 0.8 m in depth with an exposed soil surface of 0.22 m2 and a diameter of 53.8 cm (see Fig. 1). These containers were sufficiently deep to accommodate the plant rooting depth, with about six to eight plants per container. To achieve similar conditions inside and outside the lysimeters, the following procedure was followed for each lysimeter: 1. Soil was removed from the location of the lysimeter in 0.25-m (9.85 inch) depth intervals. The soil from each depth interval was stockpiled separately. 2. The polyethylene containers were placed in the hole 3. A 20-cm layer of gravel was placed in the bottom of the polyethylene tank and a polyvinyl chloride tube was placed in the bottom to remove the percolated water during operation along with a separate tube for soil moisture data collection (Fig. 1). 4. The stockpiled soil was placed in the container in the reverse order that the soil was excavated. Each layer was carefully compacted until the original 0.25-m layer thicknesses were achieved. After the container was full, the surface runoff collector and the access tube to measure the volumetric moisture content were installed. The runoff collector consisted of a small tank (0.20 m deep) connected to the lysimeter through a plastic gutter (Fig. 1). The lysimeters were located within plots measuring 7 m wide by 61 m long, with the long dimension oriented in the direction of the prevailing wind, southwest to northeast. Daily rainfall was measured within each lysimeter with a manual rain gauge and compared with an automated tipping bucket rain gauge associated with the weather station used to estimate reference evapotranspiration (ETo). For this research, an automatic weather station (WatchDog-900ET, Spectrum Technologies) was placed within an adjacent field planted with a reference crop (Panicum maximum Jacq. and Clitoria termatea L. grasses) with

Field experiments were performed at the Experimental Station of the University of Puerto Rico in Juana Diaz, PR, which is located in south-central Puerto Rico, at 18º1´ N and 66º22´ W, with an elevation of 21 m above sea level, within a semiarid climatic zone (Goyal and Gonzalez, 1989). The field experiments were planted on 15 Feb. 2006 and on 17 Jan. 2007 and meteorological data during the experiments were recorded (Table 1) using an automatic weather station (WatchDog-900ET, Spectrum Technologies, Plainfield, IL). The automatic weather station measured basic weather information, including solar radiation, temperature, humidity, and wind speed and direction every 10 min. The soil was classified as a San Anton clay loam (a fine-loamy, mixed, superactive, isohyperthermic Cumulic Haplustoll) containing 44% silt, 30% sand, 26% clay, and 1.3% organic matter within the first 40-cm depth. The soil has a volumetric water content of 0.30 m3 m–3 at field capacity and 0.19 m3 m–3 at the wilting point (Soil Conservation Service, 1987) at the 40-cm depth. In 2007, a small-plot field experiment was planted using genotypes BAT 477, Morales, SEN 3, SEN 21, SER 16, and SER 21. The genotypes were planted in 4-m rows, 1 m apart, with five replications in a split-plot design. The main plot was the irrigation treatment and the split plot was the genotype. In addition, in 2006 and 2007, larger plots (7 by 61 m) of two genotypes, Morales and SER 16, were planted for detailed studies of evapotranspiration using lysimeters and weather stations. These plots were planted in a split-plot design with three replications. Field yield component data were collected from five-row plots 2.0 m in length. In both years, treatments were planted side by side, with one block grown under drought stress and the other under reduced stress conditions using carefully controlled drip irrigation. In this study, reduced stress means that drought stress was present but at lower levels than for the drought stress treatment. Intermittent drought stress was applied in 2006 and 2007 from the beginning of reproductive development (R1) to harvest, and irrigation was administered when the soil moisture content reached 25% of field capacity (FC), generally twice a week (see irrigation and rainfall data in Table 2). Volumetric moisture content was measured at the 20- and 40-cm depths using a profile probe type PR2 sensor (Delta-T Devices) through two access tubes installed in each main plot. Water supplied through irrigation was measured using a cumulative electronic digital flow meter (GPI Inc., Conyers, GA) and was recorded manually at the beginning and end of 1208

Determination of Crop Evapotranspiration


Table 2. Water applied and rainfall in field experiments in Juana Diaz, Puerto Rico, in 2006 and 2007. Date

Developmental stage

Irrigation Nonstress Stress

Rainfall mm

Total water applied (irrigation + rainfall) Nonstress Stress

2006 14 Feb. 17 Feb. 22 Feb. 25 Feb. 27 Feb. 3 Mar. 11 Mar. 14 Mar. 16 Mar. 25 Mar. 29 Mar. 8 Apr. 11 Apr. Total

V1 V2 V3 V4 V5 V8 R1 R2 R2 R4 R5 R8 R9

21 19 31 3 12 20 15 24 0 22 33 8 15 223

19 20 32 4 12 20 0 6 5 0 17 0 4 139

3 7 3 0 0 0 56 0 34 37 3 106 0 249

24 26 34 3 12 20 71 24 34 59 36 114 15 472

24 Jan.

V1

10

31 Jan. 1 Feb. 5 Feb. 7 Feb. 13 Feb. 15 Feb. 21 Feb. 24 Feb. 26 Feb. 1 Mar. 5 Mar. 6 Mar. 9 Mar. 12 Mar. 15 Mar. 20 Mar. 23 Mar. 28 Mar. 30 Mar. Total

V2 V2 V3 V3 V4 V5 V6 R1 R2 R3 R4 R4 R5 R6 R6 R7 R8 R8 R9

22 0 25 26 40 27 25 11 13 30 34 0 60 27 32 15 15 0 0 412

22 27 35 4 12 20 56 6 39 37 20 106 4 388

8

0

10

8

15 23 26 23 14 29 21 0 0 10 23 9 20 13 0 15 9 0 0 258

0 0 0 0 0 0 2 0 0 0 0 0 0 0 1 0 20 14 18 55

22 0 25 26 40 27 27 11 13 30 34 0 60 27 33 15 35 14 18 467

15 23 26 23 14 29 23 0 0 10 23 9 20 13 1 15 29 14 18 313

2007

enough fetch and sufficient water supply during the research period. The canopy height was maintained close to 0.15 m throughout the growing season. The automatic weather station measured basic weather information, including solar radiation, temperature, humidity, and wind speed and direction every 10 min. The ETo was calculated using the Penman–Monteith equation recommended by the FAO (Allen et al., 1998). Water from RO and DP was removed from the collection containers periodically by means of a small vacuum pump (4UN26, SHURflo, Cypress, CA). The total depth of water in the soil profile was related to the soil moisture content as follows: Si = Σ (θv,i,0–10Z0–10 + θv,i,10–20Z10–20 + … + θv,i,50–60Z50–60), where Si is the depth of soil water on the ith day (mm), θv,i is the volumetric soil moisture content on the ith day, and Z is the thickness of the soil layer (10 cm). The depth intervals are specified for each of the six layers considered, for example, 0-10 cm indicates the soil interval from 0 to 10 cm.

Volumetric soil moisture was measured using a profile probe type PR2 sensor (Delta-T Devices). The access tube was placed vertically in the middle of the lysimeter. The experiment had 12 lysimeters, with six per water treatment (drought stress and nonstress) distributed between the Morales and SER 16 genotypes. Crop evapotranspiration was also derived using a second method, by means of the generalized Penman–Monteith (GPM) equation (Allen et al., 1998) using direct measurements of net radiation, soil heat flux, air temperature and humidity, wind speed, aerodynamic resistance and bulk surface resistance (as described by Harmsen et al., 2009) during the entire growing season for each of the main plots and genotypes, using in total four weather stations (2 genotypes × 2 water levels). The canopy or bulk surface resistance (rs) was calculated using the equation proposed by Szeicz and Long (1969), rs = rL/LAIactive, where LAIactive is the active leaf area index (m2 leaf area m–2 soil surface), equal to 0.5 times the leaf area


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i.e., where the temperature, atmospheric pressure, and wind velocity distribution follow nearly adiabatic conditions (no heat exchange). A study of surface and aerodynamic resistance performed by Kjelgaard and Stockle (2001) determined that Eq. [3] produced reliable estimates of ra for crops with low plant heights. The bulk surface resistance (rs) was estimated using the method of Ortega-Farias et al. (2004):

rs =

Fig. 1. Cross-section schematic of lysimeter design.

index, and rL is the stomatal resistance (s m–1), which is the total resistance from the cell surface to the exterior leaf surface (Wenkert, 1983) and is one of the most sensitive elements in evapotranspiration under drought stress conditions. The rL was measured every 2 h using the adaxial surface, from 0700 to 1700 h, to obtain a reasonable average value for each phenological growing phase for each genotype and water level. Two leaf porometers were used: AP4-UM-3 (Delta-T Devices) during 2006, and SC-1 (Decagon Devices, Pullman, WA) during 2007. Readings were taken once per week. The GPM equation for actual evapotranspiration is

ET =

D( Rn -G ) +ra c p éë(es - ea ) ra ùû l D+ g éê1 + (rs ra )ùú ë û

{

}

[2]

where Δ is the slope of the vapor pressure curve (kPa ºC–1), Rn is net radiation (MJ m–2 h–1), G is the soil heat flux density (MJ m–2 h–1), ρa is air density (kg m–3), cp is the specific heat of air (MJ kg–1 ºC–1), γ is the psychrometric constant (kPa ºC–1), es is the saturated vapor pressure, ea is the actual vapor pressure (kPa), λ is the latent heat of vaporization (2.45 MJ kg–1), ra is aerodynamic resistance (s m–1), and rs is bulk surface resistance (s m–1). In this study, the aerodynamic resistance was estimated from the following equation (Allen et al., 1998):

ln é( zm - d ) zom ùû ln éë( z h - d ) zoh ùû ra = ë k 2 u2

[3]

where zm is the height of the wind measurement (2 m), zh is the height of the humidity measurement (2 m), d is the zero plane displacement height (calculated as 0.67 times the crop height), zom is the roughness length governing momentum transfer (0.123 h), zoh is the roughness length governing the transfer of heat and vapor (0.1 zom), k is von Karman’s constant (0.41), and h is the crop height. The crop height (h) was measured for each genotype once per week, and polynomial models were developed to estimate daily values of h as a function of the day of the year. The value of ra was calculated at 1-min time intervals. Allen et al. (1998) reported that Eq. [3] and the associated estimates of d, zom, and zoh are applicable for a wide range of crops. Equation [3] is restricted to neutral stability conditions, 1210

ra c p VPD q FC -q WP D( Rn -G ) q i -q WP

[4]

where θFC is the volumetric moisture content at field capacity (fraction), θWP is the volumetric moisture content at the wilting point (fraction), and θi is the volumetric soil moisture content in the root zone (fraction) measured daily. Meteorological data were recorded by a Campbell Scientific CR10X datalogger (Campbell Scientific, Logan, UT) every 10 s. Temperature and relative humidity were measured using a Vaisala HMP45C sensor (Vaisala, Helsinki, Finland). Net radiation was measured using an NR Lite net radiometer (Campbell Scientific). Wind speed was measured 3 m above the ground using a Met One 034B wind speed and direction sensor (Met One Instruments, Grants Pass, OR). The wind speed at 3 m was adjusted to the 2-m height using the logarithmic relation presented by Allen et al. (1998). Soil water content was measured using a CS616 water content reflectometer (Campbell Scientific). The CS616 sensor was placed at the 15-cm depth (connected to a datalogger) and also a PR2 type profile probe (Delta-T Devices) was used to make soil moisture reading at two depths, 0 to 20 and 20 to 40 cm. Soil temperature was measured using two TCAV averaging soil temperature probes (Campbell Scientific), and the soil heat flux at 8 cm below the surface was measured using an HFT3 soil heat flux plate (Campbell Scientific). The soil temperature readings were used to correct the soil heat flux calculations. The leaf area index (LAI) was estimated using a nondestructive method developed by Ramirez-Builes et al. (2008) for these genotypes, which estimates the leaf area (LA, cm2) using the maximum single leaf width (W, cm). Five rows were selected from each treatment and within each row five plants were randomly selected. All leaves of the selected plants were measured. The models used were: LA = 9.35W – 20.32 for SER 16, and LA = 7.80W – 14.59 for Morales. The LAI was estimated on a weekly basis based on the plant density. Water Use Efficiency and Transpiration Efficiency Calculation In the field trials, WUE was estimated as the ratio of the seed yield per unit of evapotranspiration and as the ratio of the total biomass per unit of evapotranspiration (Howell et al., 1998). Additionally, HI was estimated as the ratio of seed yield to total aboveground biomass (Hammer and Broad, 2003; Howell et al., 1998). In this study, crop potential transpiration was assumed to be approximately equal to the basal crop evapotranspiration coefficient (ETcb) multiplied by the reference evapotranspiration, (T ~ ETcb = KcbETo). The values of ETo, T, and Kcb (defined below) were estimated daily for each genotype and water level treatment. Dry matter and T are expressed in kilograms per square meter, while k is expressed in pascals. The dual crop coefficients are the basal crop coefficient (Kcb) and soil evaporation coefficient (Ke). The coefficients Kcb and Ke Agronomy Journal • Volume 103, Issue 4 • 2011

relate the potential plant transpiration and soil evaporation, respectively, to the crop evapotranspiration. Calculations of Ke and Kcb were made using the FAO-56 approach (Allen et al., 1998), as

ET K cb = c - K e ETo

[5]

The soil evaporation coefficient (Ke) was estimated as a function of the field surface wetted by irrigation ( few) and Kc:

K e = f ew K c

[6]

and the few values were estimated as a minimum between the fraction of the soil that is exposed to sunlight and air ventilation and serves as a source of soil evaporation (1 – fc, where fc is the soil fraction covered by vegetation) and the fraction of the soil surface wetted by irrigation or precipitation ( fw)], which were measured twice per week:

f ew = min (1- f c ; f w )

[7]

and for drip irrigation:

f ew = min ëé1- f c ;(1- 0.67 f c ) f w ûù

[8]

Because the water source was drip irrigation, the value of fw was estimated as a cover crop fraction:

f w = 1-

2 fc 3

[9]

and on days with rain was equal to 1.0. Normality and variance homogeneity tests were completed as well as an analysis of variance. Means were separated using Tukey and LSD multiple range tests at P < 0.05, using the Infostat 2003 Version 3 statistical program (InfoStat, 2003). RESULTS AND DISCUSSION Climatic conditions varied across experiments in the greenhouse and field. In the greenhouse, the average temperature was 2 to 3ºC higher, the relative humidity was 13 to 20% higher, and the solar radiation and wind speed were both lower than for the field environment, resulting in stress due to high temperature and humidity (Table 1). In the field trails, the conditions in 2006 were cooler than during the same period in 2007. During 2007, drought stress was more severe, resulting in greater differences in total evapotranspiration (ETc) across treatments. Crop Evapotranspiration The ETc measured using drainage lysimeters was correlated with ETc estimated using the GPM model (correlation = 0.81, P = 0.05). The overall average evapotranspiration across treatments and genotypes was 154 mm for the lysimeter method and 160 mm for the GPM method (data not shown). Using drainage lysimeters under reduced stress conditions, the ETc of Morales totaled (from V2–R9 phenological phases) 211 mm in 2006 and 215 mm in 2007, compared with 172 and 190 mm in 2006 and 2007, respectively, using the GPM model (Table 3). The measured ETc for SER 16 totaled 142 mm in 2006 and 153 mm in 2007 compared with the GPM model estimates of

Table 3. Cumulative evapotranspiration from V2 to R9 phenological phases† for two common bean genotypes, Morales and SER 16, measured using the water balance (lysimeter) and energy balance (generalized Penman–Monteith, GPM) methods in the field in Juana Diaz, Puerto Rico. Evapotranspiration Drought stress Reference evapotranspiration Genotype Lysimeter GPM Lysimeter GPM (GPM) mm 2006 Morales 211 (5.6)‡ 172 167 (20.2) 155 256 SER 16 142 (5.9) 147 100 (6.8) 158 256 2007 Morales 215§ 190 140 (26.6) 152 263 SER 16 153 (0.7) 166 107 (37.7) 137 263 Reduced stress

† V2, one node above primary leaf node; R9, maturity with 80% of pods ripe. ‡ Mean with SD in parentheses; no SD provided for the GPM method because there was one weather station per genotype–treatment combination. § Two of the three lysimeters had poor plant stand, thus the SD could not be calculated.

147 and 166 mm for 2006 and 2007, respectively. The lower ETc values for SER 16 compared with Morales were associated with lower plant densities for SER 16 due to a reduced plant stand, thus comparisons could not be made. Other studies have shown higher water requirements for dry bean for a 90- to 100-d season ranging from 350 to 500 mm depending on the soil, climate, and cultivar (Allen et al., 2000). Calvache et al. (1997) reported a crop water requirement of 447 mm for dry bean for a 122-d season, while Muñoz-Perea et al. (2007) reported 318 mm for the cultivar NW 63 and 457 mm for ‘Othello’ under well-watered conditions, and 270 mm for Othello and 338 mm for the Common Pinto landrace under drought stress conditions in Kimberly, ID. Nielsen and Nelson (1998) reported ET values ranging from 265 to 455 mm for black bean grown in eastern Colorado with 183 mm of irrigation and no precipitation. The relatively low seasonal crop evapotranspiration values in this present study are associated with a number of factors including: a shorter crop season, 75 and 78 d in 2006 and 2007, respectively; lower plant density; climatic factors, such as low evaporative demand; and the use of drip irrigation, which reduces soil evaporation. To take the shorter season into effect, daily ET rates were also calculated. Adams et al. (1985) reported that dry bean required 25 to 30 mm of water per week (3.6–4.3 mm d–1), and that dry bean water use increased from 1.3 (during vegetative development) to 6.3 mm d–1 (during pod development) (North Dakota State University Extension Service, 2003, p. 78–85). In this study, the ETc increased from 0.7 mm d–1 during vegetative development to 5.1 mm d–1 during pod development for Morales in 2006 under reduced stress conditions, and from 0.6 to 4.6 mm d–1 in 2007. For SER 16, ETc increased from 0.4 mm d–1 in the vegetative growing phase to 5.1 mm d–1 in the pod-filling phase in 2006, and from 0.3 to 6.7 mm d–1 in 2007 (data not shown). Low evapotranspiration rates on specific days during the experiment (data not shown) were associated with high surface resistance (rs) values (see surface resistance explanation above). Low values of aerodynamic resistance (ra) were directly related to high wind velocities (5.0–8.0 m s–1) during that period, which probably induced stomatal closure (e.g., Davies, 1978; Dixon and Grace, 1984; Smith, 1980). Davies (1978) found that stomata closed with high wind speeds, resulting in increasing rL and subsequently


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Table 4. Analysis of water use efficiency (WUE) calculated as seed yield per unit of water applied for six common bean genotypes grown under three water treatments and in three greenhouse experiments in Mayaguez, Puerto Rico, during 2005 and 2006. 2005 Genotype Treatment† July–Sept. BAT 477

Morales

SEN 21

SEN 3

SER 16

SER 21

Mean

nonstress stress level 1 stress level 2 nonstress stress level 1 stress level 2 nonstress stress level 1 stress level 2 nonstress stress level 1 stress level 2 nonstress

WUE 2006 July–Sept.

2006 Oct.–Dec.

g seed L–1 water applied 0.16 ghi‡ 0.59 pqrst 0.43 klmnopqr 0.18 ghij 0.64 rstuv 0.59 pqrst 0.17 ghij 0.40 jklmnopq 1.16 abc 0.06 g 0.43 klmnopqr 0.55 nopqrs 0.14 gh 0.62 qrstu 0.83 uvwxy 0.06 g 0.52 klmnopqr 1.29 bcd –§ 0.57 opqrst 0.79 tuvwx – 0.14 gh 0.91 wxyz – 0.21 ghijk 0.50 klmnopqr – 0.84 uvwxy 1.20 abc – 1.01 xyza 1.37 cd – 1.03 yza 1.33 cd 0.25 ghijk 0.86 vwxyz 1.07 zab

stress level 1 0.33 hijklmn stress level 2 0.28 ghijkl nonstress 0.24 ghijk stress level 1 0.31 hijklm stress level 2 0.51 lmnopqr 0.22

0.74 stuvw 0.37 ijklmnop 0.79 tuvwx 0.93 wxyz 1.05 yza 0.65

1.51 c 0.35 hijklmno 1.01 xyza 1.45 c 1.37 cd 0.98

† Nonstress, 80% of the daily available water (DAW) applied; stress level 1, 50% of the DAW applied preflowering and 60% applied after flowering; stress level 2, 20% of the DAW applied preflowering and 40% applied after flowering. Four replicates were completed under each treatment regime. ‡ Means followed by the same letter are not significantly different according to the LSD test at a = 0.05. § Not tested in the Dec. 2005 trial in which the WUE values were lowest, on average, of the three trials.

increasing rs. Changes in rs are also directly associated with rL and LAI. Low levels of drought stress during 2006 were not sufficient to generate significant changes in LAI or rs; however, larger differences in LAI, rL, and subsequently rs were observed under the more severe drought stress conditions during 2007. Thus, application of these physiological parameters may be more useful under higher levels of drought stress. Maximum ETc rates occurred after pod initiation (R3), and maximum LAI occurred at the R4 growth stage (4.2 and 3.0 m2 m–2 for Morales in 2006 and 2007, respectively, and 1.7 and 1.8 m2 m–2 for SER 16 in 2006 and 2007, respectively). The differences in LAI are probably associated with differences in plant densities for the two genotypes, thus comparisons between the two genotypes were not made. Water Use Efficiency In the analysis of WUE from the three water treatment levels and the three greenhouse trials, there were differences between trials and genotypes. The SEN 3 and SER 21 genotypes showed higher WUE values in specific treatments and trials (Table 4). It is important to note, however, that SEN 3 and SEN 21 were tested in only two out of the three trials and were not included in the July 2005 trial, in which the WUE values were lowest, on average, of the three trials. In addition, HI (Table 5) varied with genotype and corresponded with the WUE response. The HI of SER 21 ranged from 0.25 to 0.54 and of SEN 3 from 0.38 to 0.51, while the HI of BAT 477 ranged from 0.15 to 0.34 and of Morales 1212

Table 5. Analysis of the harvest index (HI) for six common bean genotypes grown under three water treatments and in three greenhouse experiments in Mayaguez, Puerto Rico, during 2005 and 2006. 2005 Genotype Treatment† July–Sept. BAT 477

Morales

SEN 21

SEN 3

SER 16

SER 21

Mean

nonstress stress level 1 stress level 2 nonstress stress level 1 stress level 2 nonstress stress level 1 stress level 2 nonstress stress level 1 stress level 2 nonstress

HI 2006 July–Sept.

2006 Oct.–Dec.

kg seed kg–1 biomass 0.26 nopqr‡ 0.27 nopqr 0.19 jklmn 0.23 klmnop 0.29 opqrs 0.21 klmno 0.15 hijk 0.15 hijk 0.34 qrstuvw 0.16 hijklm 0.24 klmnop 0.24 klmnop 0.15 hijk 0.26 mnopq 0.32 pqrtsuv 0.04 g 0.18 ijklmn 0.40 tuvwxy –§ 0.36 rstuvwx 0.42 vwxyz – 0.07 gh 0.42 vwxyza – 0.09 ghi 0.21 klmno – 0.45 xyzab 0.50 yzab – 0.38 stuvwx 0.51 zab – 0.40 uvwxy 0.39 tuvwx 0.39 tuvwx 0.39 tuvwx 0.42 vwxyza

stress level 1 0.31 pqrstu 0.36 rstuvwx stress level 2 0.25 mnopq 0.15 hijkl nonstress 0.35 qrstuvw 0.43 wxyza stress level 1 0.25 lmnopq 0.41 vwxyz stress level 2 0.30 opqrst 0.42 vwxyz 0.24 0.29

0.51 ab 0.10 ghij 0.49 xyzab 0.54 b 0.39 stuvwx 0.37

† Nonstress, 80% of the daily available water (DAW) applied; stress level 1, 50% of the DAW applied preflowering and 60% applied after flowering; stress level 2, 20% of the DAW applied preflowering and 40% applied after flowering. Four replicates were completed under each treatment regime. ‡ Means followed by the same letter are not significantly different according to the LSD test at α = 0.05. § Not tested in the Dec. 2005 trial in which the WUE values were lowest, on average, of the three trials.

from 0.04 to 0.40. Thus, SER 21 and SEN 3 were able to maintain relatively high seed yield efficiency under drought stress. The most severe drought stress, lowest WUE, and highest drought intensity index [DII = 1 – (Xs/Xp), where Xs and Xp are the mean yield for all genotypes per trial under stress and nonstress conditions, respectively] was observed in the experiment conducted from July to September 2005. The reduced performance in this trial could be related to the higher mean air temperature observed during that period (27.6ºC) compared with mean temperatures of 26.0 and 26.6ºC in the other two trials. In this experiment, genotypes SER 21 and SER 16 showed significantly higher WUE in specific treatments. The highest values for WUE were found in the October to December 2006 trial, which is probably associated with the lowest average temperatures (26.0ºC) of the three trials. In the greenhouse environment, where root growth is limited to the volume of the pot, there are few mechanisms for drought stress avoidance (such as deep taproots). Under field conditions, drought stress was more severe in 2007 (Table 6). In 2007, 33% less water was applied in the drought stress treatment than the reduced stress treatment and the DII was 0.72, while in 2006, 18% less water was applied compared with the reduced stress treatment and the DII was 0.31. The severity in the drought stress experiment in 2007 may also have been due to higher air temperatures during the preflowering and pod-filling periods, where the mean air temperature was 25.2ºC in 2007, compared with 24.5ºC during the same period Agronomy Journal • Volume 103, Issue 4 • 2011

Table 6. Yield components, evapotranspiration (ET), and water use efficiency (WUE) for two common bean genotypes grown under drought stress and reduced stress conditions in Juana Diaz, Puerto Rico in 2006 and 2007. Field data were collected from fiverow plots of 2.0 m in length, with three replications. 2006

Variable Seed yield, kg ha–1 Biomass, kg ha–1 Plant density, no. m–2 Harvest index‡ Pods, no. m–2 ET, mm WUE§, kg ha–1 mm–1 WUE¶, kg ha–1 mm–1 Yield reduction, % Geometric mean#, kg ha–1

Morales Reduced Drought stress stress 1954 (297)† 1316 (391) 4205 (579) 2897 (745) 13.6 (4.1) 14.0 (2.6) 0.47 (0.04) 0.45 (0.04) 221 (0.8) 169 (41.1) 172.2 154.8 24.4 18.7 11.3 8.5 33 1604

2007 SER 16 Reduced Drought stress stress 2020 (231) 1444 (323) 3594 (329) 2443 (497) 6.4 (6.0) 6.5 (1.7) 0.56 (0.02) 0.59 (0.02) 179 (23.5) 154 (22.7) 147.2 157.6 24.4 15.5 13.6 9.2 29 1708

Morales Reduced Drought stress stress 859 (168) 210 (118) 2318 (292) 1015 (252) 13.2 (4.4) 14.7 (2.8) 0.37 (0.03) 0.21 (0.04) 138 (25.1) 56 (14.2) 189.9 151.8 12.2 6.7 4.5 1.4 76 425

SER 16 Reduced Drought stress stress 691 (255) 226 (67) 1615 (473) 717 (121) 6.0 (2.8) 6.0 (0.3) 0.43 (0.06) 0.32 (0.04) 90 (29.0) 44 (9.0) 166.3 137.1 9.7 5.2 4.2 1.6 67 395

† Means with SD in parentheses. ‡ Harvest index calculated as the ratio of grain yield to biomass yield; biomass yield was determined at 75 and 78 d after planting in 2006 and 2007, respectively, using root, stem, and leaf material. § WUE computed as biomass per unit of evapotranspiration. ¶ WUE computed as seed yield per unit of evapotranspiration. # Geometric mean = (YsYp)1/2 , where Ys is yield under stress and Yp is yield under reduced stress.

in 2006. Additionally, during pod filling, windy conditions imposed an additional physiological stress during several days. The lower stress in 2006 was associated with substantial rainfall received during the growing season. In 2006, there was 249 mm of rainfall, whereas in 2007 there was 55 mm of rainfall. In the field, the seed yields of SER 16 and Morales were not statistically different, indicating that yield compensation probably occurred with SER 16, due to its lower plant density (Table 6). Drought stress reduced the biomass, seed yield, and HI for both genotypes in both years, with the most marked effect found in 2007. The marked reduction in yield in 2007 from 2006 is evident in the geometric mean (GM): the GM of Morales was 1604 kg ha–1 and SER 16 was 1708 kg ha–1 in 2006 and Morales was 425 kg ha–1 and SER 16 was 395 kg ha–1 in 2007. Favorable climatic conditions in 2006 resulted in higher WUE values for both genotypes (Table 6), while during the 2 yr, seed yield based WUE ranged from 1.4 to 13.6 kg ha–1 mm–1. Morales showed higher WUE than SER 16 under drought stress when based on biomass, while WUE based on seed yield was quite similar between the two genotypes, although comparison is difficult due to differences in plant stand. Muñoz-Perea et al. (2007) reported values of mean WUE in bean, under favorable climate conditions in Kimberly, ID, of 8.7 kg ha–1 mm–1 for nonstress conditions and 9.8 kg ha–1 mm–1 for stress conditions. Under unfavorable climatic conditions (high stress levels), they reported WUE values ranging from 4.4 kg ha–1 mm–1 for the cultivar Othello to 1.1 kg ha–1 mm–1 for the landrace Common Pinto. Thus, in this study, higher levels of stress in the 2007 field trial resulted in greater reductions in WUE for both genotypes, while both genotypes responded similarly with reductions in WUE under stress vs. nonstress in both field trials.

a previous study using weighing lysimeters in the semiarid tropics of South Africa, where k was found to be 3.26 ± 0.25 g kPa kg–1 (Ogindo and Walker, 2004). The k values under nonstress are also similar to those of other C3 groups (Kemanian et al., 2005). For both years, both genotypes showed large reductions in k under drought stress conditions, where the difference between knonstress and kstress was 2.0 Pa in 2006 and 2.3 Pa in 2007 for Morales, and 1.6 Pa in 2006 and 1.2 Pa in 2007 for SER 16. Genotype variability in k has not been widely reported and studied in common bean. Additional research needs to be completed to evaluate differences between genotypes and the correlation with yield components. SUMMARY AND CONCLUSIONS In this study, crop evapotranspiration was estimated with the generalized Penman–Monteith model and measured with drainage lysimeters for two common bean genotypes, under drought stress and reduced stress conditions. Both estimated and measured evapotranspiration were lower than previously published values Table 7. Estimated mean daytime vapor pressure deficit (VPD) and transpiration efficiency coefficient (k) for two common bean genotypes, Morales and SER 16, under drought stress and reduced stress conditions during 2 yr (2006 and 2007) in the field in Juana Diaz, Puerto Rico. Single measurements were taken from a weather station located in each genotype–treatment combination. Genotype

SER 16 Morales

Coefficient for Transpiration Use Efficiency The results for TE indicate relatively large differences between water levels and experiments, with k ranging from 1.0 to 2.6 Pa under drought stress and from 2.2 to 4.2 Pa under nonstress conditions (Table 7). The estimated k was similar to that found in

SER 16 Morales


Treatment

Mean daytime VPD Pa 2006 reduced stress 1318 drought stress 1289 reduced stress 1348 drought stress 1329 2007 reduced stress 1452 drought stress 1464 reduced stress 1452 drought stress 1499

k

4.2 2.6 3.8 1.8 2.2 1.0 3.6 1.3

1213

and may indicate the need for additional studies for different agroecological zones, such as the tropics, which vary in length of crop season, humidity, etc. The results from this study indicate that under greenhouse water-limited conditions, the genotypes SEN 3 and SER 21 showed better performance in terms of WUE under specific treatments and thus could be used for further research and for the improvement of this trait in breeding programs. Under field conditions, both Morales and SER 16 showed large reductions in TE and WUE under drought stress conditions. ACKNOWLEDGMENTS This research was supported by the USDA-TSTAR Program (TSTAR-100), and the University of Puerto Rico received additional support from NASA-EPSCoR (NCC5-595). We thank Abraham Montes, Adolfo Quiles, and Carlos Almodovar for their assistance with the field trials. Mention of trade names or commercial products in this article is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the USDA. REFERENCES Adams, M.W., D.P. Coyne, J.H.C. Davis, P.H. Graham, and C.A. Francis. 1985. Common bean (Phaseolus vulgaris L.). p. 433–476. In R.J. Summerfield and E.H. Roberts (ed.) Grain legume crops, Collins, London. Allen, G.R., L.S. Pereira, D. Raes, and M. Smith. 1998. Crop evapotranspiration: Guidelines for computing crop water requirements. Publ. 56. FAO, Rome. Allen, R.G., C.D. Yonts, and J.L. Wright. 2000. Irrigation to maximize bean production and water use efficiency. p. 71–92. In S.P. Singh (ed.) Bean research, production, and utilization. Proc. Idaho Bean Workshop. Univ. of Idaho, Moscow. Beaver, J.S., and P.N. Miklas. 1999. Registration ‘Morales’ small white bean. Crop Sci. 39:1257. Beebe, S., and B. McClafferty. 2006. Biofortified beans. Available at www. research4development.info/PDF/Outputs/Misc_Crop/beans.pdf (verified 18 Apr. 2011). HarvestPlus, CIAT, Cali, Colombia. Beebe, S., I.M. Rao, M.W. Blair, and J.A. Acosta-Gallegos. 2011. Phenotyping common beans for adaptation to drought. p. 315–342. In P. Monneveux and J.-M. Ribaut (ed.) Drought phenotyping in crops: From theory to practice. Generation Challenge Progr., Texcoco, Mexico. Boman, B.J. 1991. Alfalfa ET measurements with drainage lysimeters. p. 264– 271. In R.G. Allen et al. (ed.) Lysimeter for evapotranspiration and environmental measurements: Proc. Int. Symp. on Lysimetry, Honolulu, HI. 23–25 July 1991. Am. Soc. Civ. Eng., Washington, DC. Boutraa, T., and F.E. Sanders. 2001. Influence of water stress on grain yield and vegetative growth of two cultivars of bean (Phaseolus vulgaris L.). J. Agron. Crop Sci. 187:251–257. doi:10.1046/j.1439-037X.2001.00525.x Broughton, W.J., G. Hernandez, M. Blair, S. Beebe, P. Gepts, and J. Vanderleyden. 2003. Beans (Phaseolus spp.): Model food legumes. Plant Soil 252:55–128. doi:10.1023/A:1024146710611 Calvache, M., K. Reichardi, O. Bacchi, and D. Dourado-Neto. 1997. Deficit irrigation at different growth stages of the common bean (Phaseolus vulgaris L., cv. Imbabello). Sci. Agric. 54(Spec.):1–16. Caspari, H.W., S.R. Green, and W.R.N. Edwards. 1993. Transpiration of wellwatered and water-stressed Asian pear trees as determined by lysimetry, heat-pulse, and estimated by a Penman–Monteith model. Agric. For. Meteorol. 67:13–27. doi:10.1016/0168-1923(93)90047-L Condon, A.G., R.A. Richards, G.J. Rebetzke, and G.D. Farquhar. 2004. Breeding for high water-use efficiency. J. Exp. Bot. 55:2447–2460. doi:10.1093/jxb/erh277

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