Environmental and Experimental Botany 68 (2010) 165174

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Environmental and Experimental Botany

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Strawberry plant fruiting efciency and its correlation with solar irradiance, temperature and reectance water index variation
Hong Li a,b, , Tingxian Li c , Robert J. Gordon d , Samuel K. Asiedu a , Kelin Hu b
a

Nova Scotia Agricultural College, Department of Plant and Animal Sciences, Truro, Nova Scotia, B2N 5E3, Canada China Agricultural University, Department of Soil and Water Sciences, Beijin 100094, China Ministry of Sustainable Development, Environment and Parks of Quebec, Sustainable Development and Ecological Inheritance Services, Quebec City, Quebec, G1R 5V7, Canada d University of Guelph, School of Environmental Sciences, Guelph, Ontario, N1G 2W1, Canada
b c

a r t i c l e

i n f o

a b s t r a c t
Uneven light distribution and low water holding capacity are two constraints limiting strawberry (Fragaria ananassa Duch.) production in coastal northern Atlantic areas. A study was conducted in a commercial strawberry production eld characterized by rapid internal soil drainage and undulating land features in Nova Scotia. The objectives were to examine the uneven distribution patterns of solar irradiance (IRR), temperature and soil water content (SWC) and quantify correlations of these physical variables with strawberry fruit yield, plant reectance water index (WI) and leaf chlorophyll. Strawberry row orientation was along the eld aspect in the northsouth (NS) direction for maximizing plant sunlight exposure and spring rainfall drainage. The measurement design consisted of a nested grid with ve transects. Results showed that solar radiation incident upon the canopy was signicantly higher (mean IRR 779820 W m2 ) in the shoulder and slope areas compared to the mean IRR of 709 W m2 in downslope area (P < 0.001), where higher SWC and lower temperature stimulated strawberry fruit bearing. Signicantly higher reectance WI was related to low strawberry yield (R2 = 0.55, P < 0.05). Strawberry fruit yield was positively correlated to normalized difference vegetation index, ratio nitrogen vegetative index and leaf chlorophyll (0.46 < R2 < 0.61, P < 0.05). Distribution patterns and correlations between strawberry fruit yield and physical variables suggested that IRR and water stress occurring with the inuence of high topographic features resulted in reduced strawberry fruit bearing ability. It was suggested that the NS row orientation along the aspect would help sunlight capture but not water holding for strawberry plant fruit bearing needs. A new planting design for alternative orientation of rows (NESW or WE) and drip irrigation should be tested for light and water management in soils with natural constraints. 2009 Elsevier B.V. All rights reserved.

Article history: Received 7 July 2009 Received in revised form 4 November 2009 Accepted 1 December 2009 Keywords: Light Planting design Strawberry fruit Topographic features Water

1. Introduction Strawberry (Fragaria ananasa Duch.), a small fruit crop and a hybrid of two highly variable octoploid species, has adapted to extremely different environmental conditions (Heide, 1977; Rieger, 2005). In North America strawberries are grown extensively in cool areas (e.g. Nova Scotia) and also in semi-tropical regions (e.g. Florida). Full sunlight and available water are key components for producing high quality strawberry fruit (El-farhan and Pritts, 1997; Watson et al., 2002; Rieger, 2005; Klamkowski and Treder, 2008). As strawberry fruit bearing and maturity occur in a short time (2040 days after pollination) and also strawberries have shallow root systems (the plants are growing via stolons), light and water

Corresponding author. Tel.: +1 902 893 7859; fax: +1 902 897 9762. E-mail address: hli@nsac.ca (H. Li). 0098-8472/$ see front matter 2009 Elsevier B.V. All rights reserved. doi:10.1016/j.envexpbot.2009.12.001

management are critical for achieving high yield and fruit quality of strawberries. In the humid and temperate coastal areas in Nova Scotia, agricultural elds typically include rolling to hilly landforms and soils are highly permeable resulting in rapid internal drainage and precipitation is also lost by runoff (Webb et al., 1991). Rapid internal drainage can be dened as water removed rapidly through the soil prole due to a high hydraulic conductivity (between 10 and 100 m s1 ) and unless irrigated only a restricted variety of crops can be grown with a low yield (Webb et al., 1991). Traditional crops are hay, oats, barley and potatoes in this coast area. In recent years, with the adoption of irrigation technology in the region, producers have grown high-value horticultural crops such as strawberries and raspberries. However, maintaining appropriate water status in these soils is critical because of the cost for irrigation and also the potential loss of fertilizers leaching with the water through the soil prole.

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Soil water is recognized as the greatest hazard affecting systems productivity and sustainability (Blum, 1996; Grifths and Parry, 2002; Sperry et al., 2002; Li et al., 2001a, 2002, 2004, 2008). Reduced water availability induces numerous physiological and biochemical changes in plant organs (Hetherington and Woodward, 2003). Drought and NaCl stress in strawberry plant can retard the development of its reproductive organs, leading to fewer owers and fruit (Blanke and Cooke, 2004; Klamkowski and Treder, 2008; Keutgen and Pawelzik, 2009). Irrigation is often practiced following the onset of plant water stress, however, this is often too late to avoid a partial reduction in yield (El-farhan and Pritts, 1997; Li et al., 2002). Plant responses in canopy spectral reectance, transmittance or absorptance are real-time eco physiological indicators of plant water stress (Jackson, 1982; Carter and Knapp, 2001). Crop yield difference can be explained by spectral index such as relative nitrogen vegetative index (RNVI), normalized difference vegetation index (NDVI) (Jackson, 1982; Li et al., 2001a,b). Reectance water index (WI) is a spectral indicator for real-time management of plant water stress (Jackson, 1982; Penuelas et al., 1997; Claudio et al., 2006). Light, solar radiation and temperature distribution can vary signicantly under different topographic features such as elevation, aspect and slope (Rorison et al., 1986; Florinsky et al., 1994; Li et al., 2001b). Temperature is one of the most important factors affecting strawberry plant nutrient uptake (Ganmore-Neumann and Kafka, 1985) and wheat photosynthesis and grain-lling (Shah and Paulsen, 2003). High temperature (2432 C) reduces strawberry ower formation and fruit quality (Heide, 1977; Klamkowski and Treder, 2008). Temperature is associated with strawberry ower bud induction (Ito & Saito, 1962; Heide, 1977), runner, meristem-tip and leaf variegation (Watkins et al., 1990), dormancy induction (Robert et al., 1999), fruit avors (Watson et al., 2002), and membrane phospholipids (Wang and Lin, 2006). Planting orientation of rows is useful for maximizing light interception by plant canopies to achieve high yield and fruit quality (Rieger, 2005). Light and water management for soils having rolling and coarse-textured gravel characteristics that can lead to uneven distribution of light and water is a challenge for growers. Currently, no information is available for light and water management under the inuence of rolling landforms and rapid internal drainage. There was a need for understanding the relationships between solar radiation, temperature, soil water and strawberry fruit yields. In addition, plant and soil functions are often encountered for underlying environmental variables, which should be measured as a function of space in systematic grid sampling scheme (Marriott et al., 1997; Cole et al., 2001; Li et al., 2002). Several studies have addressed strawberry plant and supraoptimal temperature (or photoperiod) problems only (Ito and Saito, 1962; Heide, 1977; Ganmore-Neumann and Kafka, 1985; Watkins et al., 1990; Robert et al., 1999; Watson et al., 2002; Wang and Lin, 2006), or strawberry plant water (or salinity) problems only (Blanke and Cooke, 2004; Klamkowski and Treder, 2008; Keutgen and Pawelzik, 2009). We conducted a 2-year study in a strawberry eld in the coastal areas of Nova Scotia to quantify simultaneously the roles of solar irradiance, temperature and soil water variation in strawberry fruit setting on lands with natural rolling characters and drainage constraints. It was hypothesized that undulating landforms and natural drainage constraints can create difference in solar radiation capture, temperature and soil water distribution patterns. This can then impact strawberry plant development and fruit yield. The objectives of the study were to (i) examine the distribution patterns of solar irradiance (IRR), temperatures and SWC, and (ii) quantify strawberry plant fruiting efciency and its correlations with these physical variables and plant reectance WI, canopy spectral index and leaf chlorophyll across the landscape.

The information would be useful for understanding light, temperature, water and plant relations for growing high-value fruit crops in soils with natural constraints. 2. Materials and methods 2.1. Study site and strawberry planting description The study was conducted in an irrigated, commercial strawberry production eld (45 40 01 N, 63 54 15 W) near Glenholme in the Cobequid Bay, Nova Scotia during 20062007. The site was 1.2-ha in size with a 3-crop, 6-year rotation regime, which was 2-year grass, 3-year strawberry and 1-year corn. The soil was a gravelly, rapidly drained sandy loam, classied as Hebert (map unit He2) loam, Orthic Humo-Ferric Podzols (Webb et al., 1991). The eld, typical for the area, was characterized by an undulating land surface with a slope varying between 5 and 10% and an aspect in the northsouth (NS) direction. The eld landforms consisted of a 30-m long shoulder area, a 28-m slope and a 28m downslope at terrain along the aspect. The previous crop was 2-year perennial ryegrass (Lolium perenne L.) to improve soil quality including suppressing pests and disease fungi. In May 2005, the strawberry cv Annapolis, a late June-early July bearing variety, was transplanted in raised beds (1.2 m in dimension) for soil warming, rainfall evacuating and sunlight capture. The orientation of rows was following the aspect in the NS direction, an usual planting practice of orientation of rows for maximum plant sunlight exposure for fruit bearing and also for facilitating drainage when rainfall was more frequent in the spring. The strawberry plant spacing was 1.5 m between rows and 0.50 m apart between plants in the row. After transplanting the plants were mulched with wheat straw to conserve soil water and control weeds. The strawberry plants were fertilized based on soil tests performed in the spring and utilized regional recommendations. Irrigation was done on a rainfall compensation basis using sprinkler system with pipes installed 24 m apart across the eld. The use of sprinkle irrigation was helpful for frost protection. At the critical stage of transplant establishment, the irrigation rates were 4 L m2 per day because the newly set transplants were susceptible to even mild water stress (El-farhan and Pritts, 1997). The total irrigation water was on average 260 L m2 per season, which was in the range of irrigation recommendation for mulching strawberry (El-farhan and Pritts, 1997). For better fruit bearing, strawberry plant runners were thinned during the rst growing season. Flowering stems on the plants were consistently removed as they appeared throughout the season. The ower thinning strengthened the mother plants and main runner plants. Nutrients were applied based on soil test results and disease, insect and weed control was done according to the regional recommendation. The plants were mulched for winter protection and irrigation at the rate of 5 L m2 was done prior to mulch covering to reduce risk of cold-temperature injury. In 2006, the strawberry plants were allowed to attain a large size at full vegetative stage then allowed owers for fruit bearing from June through harvest in mid July. Irrigation was done at the rate of 4 L m2 per day (dry days) during the periods of owering, initiation of berry set through the nal enlargement of the fruit. The strawberry plants were cared for crop protection, fertilization and irrigation for fruit bearing for 2007. However, the plants were hit by an unexpected hail storm during the fruit bearing period (mid June 2007), resulting in some damages on fruit formation. 2.2. The experimental design and eld measurements The experimental design was a nested grid sampling scheme, which consisted of two transects (two strawberry rows), 7.5 m

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Fig. 1. Spatial interpolated patterns of site elevation (A), solar irradiance (B), soil water content (C), strawberry plant reectance water index (D), leaf chlorophyll SPAD readings (E) and strawberry marketable fruit yield (F).

apart, along the aspect (NS) direction, and three other transects (three strawberry rows), 24 m apart, in the westeast (WE) direction across the eld. The two NS transects were ve rows apart, covering along the shoulder, slope and downslope areas where it presented the greatest variability in elevation following the aspect. The three WE transects were parallel, with each transect in the shoulder, slope and downslope area, respectively. All measurements were taken in the 7.5 6 m grid in the NS transects, and 24 12 m grid along the WE transects. The grid area was 72 m long in the aspect (NS) direction and 72 m in the WE direction (Fig. 1). This nested grid design had an advantage of emphasis on examining the spatial variability in the areas presenting the greatest variability, as shown in Marriott et al. (1997) and Cole et al. (2001). The eld measurements were initiated in 2006 because of the plant runner and ower thinning in the rst year (2005). The measurement points were geo-referenced using a Garmin handheld GPS system (Garmin International, Olathe, KS). There were a total of 42 GPS points with 12 measurements in each NS transect and 6 measurements in each WE transect. Soil temperature, strawberry leaf and fruit temperatures were measured using an infrared thermal sensor (Spectrum Technologies, Plaineld, IL). The temperature measurements were taken at full vegetative stage, at owering and at fruit bearing stage. At each stage temperatures were measured two times in a 10-day interval.

Temperature measurements were taken simultaneously on three fruits, leaves and soils at each measurement point. Fruits and leaves for the measurements were selected at the same levels of plant heights each time. Leaf chlorophyll content was measured on the same leaves as for temperature measurements using a Minolta SPAD 502 meter (Markwell et al., 1995). Three chlorophyll measurements were taken on separate leaves at each GPS point three times at full vegetative stage, at owering and at fruit bearing stage. Air temperature data were obtained from a nearby weather station in Glenholme, 3 km away from the study site. Plant canopy multispectral reectance was detected at a wavelength between 462 and 1752 nm using a portable multispectral radiometer (MSRSYS5, CropScan, Rochester, MN), a rapid assessment taken directly on plant canopies across the eld (Li et al., 2001a). The MSRSYS5 consisted of ve up-sensors to detect incident energy and ve down-sensors to detect outgoing energy. The plantsoil target surface was sensed at 2 m distance from the sensors (looking straight down) with a 31.1 eld of view yielding a ground of 1-m2 area. The reectance measurements were taken at each of the GPS points within the grids. The spectral readings were taken at 14:00 within a time of 1530 solar zenith angle at full vegetative stage, at owering and at fruit harvest. Sensor outputs consisted of the reectance readings at the center wavelength of 485, 560, 660,

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830 and 1650 nm, respectively. The blue, green, red, near infrared (NIR) and mid infrared (MIR) bands were across a wavelength width between 452518 nm, 524596 nm, 631689 nm, 757903 nm and 15531748 nm, respectively. As a result, the wavelength width was similarly narrow, comparable within the blue, green and red bands (5772 nm) and also within the NIR and MIR bands (146195 nm). Solar irradiance (IRR), the power of electromagnetic radiation incident upon the canopy surface per unit area, was detected simultaneously with the plant reectance measurements, using the MSRSYS5 radiometer up-facing sensor at the center 560 nm (wavelength width 524596 nm). This green band was the nearest band to the peak of the solar spectrum (480 nm). The up-sensor estimated the total hemispherical irradiance or received on 1-m2 canopy surface. This green band was a narrowband (72 nm) and provided estimations with uncertainty within 5% of total solar incident radiation in clear sky conditions or in lightly cloudy conditions, veried using solar pyranometer readings. It was to note although the blue band (485 nm) was closer to the peak of the solar spectrum than the green band, the blue sensor was not chose for the solar irradiance measurements because the hemispherical blue light could drop more quickly than the green light when it was slightly cloudy (Jackson, 1982; Carter and Knapp, 2001; Claudio et al., 2006). The soil water content was measured at the depth of 00.15 m using a TDR probe (Spectrum Technologies, Plaineld, IL). A composite soil sample with three soil cores was taken at the depth of 00.15 m. Soil samples were air-dried. Soil pH was measured using pHH2 O (m/v 1:1) ratio (Li et al., 2002). Soil water availability expressed on a gravimetrical basis was also determined by drying soil samples in the oven at a temperature of 110 C (Li et al., 2004). Strawberry fruit yield was hand harvested in an area of 1-m long on the rows at each GPS point in 2006. The fruit yields were assessed neither in the rst year in 2005 (due to plant thinning) nor in 2007 (because of the hail damage). The strawberry marketable yield was obtained from marketable-size (2.5 cm) fruits with red, free of defects for each GPS point. Damaged or diseased fruits were discarded. Elevation data taken using the Garmin unit were then calibrated with the soil map unit elevation (Webb et al., 1991) to obtain the estimated elevation data for each sampling site. 2.3. Plant, water and soil data analysis and mapping Strawberry plant spectral reectance readings were calibrated with a reectance correction factor, and then converted to reectance percentage, a ratio from the down and up sensor output in mV, as described in Li et al. (2001a). Soil reectance was discriminated in the red band (center 660 nm), and plant reectance was discriminated in the NIR band (center 830 nm). Plant water holding status was estimated using the reectance data in the water band, which was the MIR band (center 1650 nm), as shown in Li et al. (2001b) and Claudio et al. (2006). The ratio vegetative index (RVI) was the ratio of NIR to red reectance (NIR/red). The NIR and green (G) reectance (NIR/G) ratio was dened as relative nitrogen vegetative index (RNVI). The normalized difference vegetative index (NDVI), a spectral vegetative index widely used in termination of plant N status, was determined by the ratio of differencing and combining reectance measured in NIR and red bands as NDVI = (NIR red)/(NIR + red), as shown in Li et al. (2001a,b). Reectance water index (WI) was estimated using the ratio of the reectance within the water band wavelength, center 1650 nm, to the nearby reectance wavelength where there was no water absorption, which was the NIR band 830 nm. The wavelength width of this 1650-nm water band (width 15531748 nm) was very close to the two most prominent water bands (1400 and 1900 nm). Water adsorption was strong in the MIR bands and plant reectance at

these wavelengths has been shown to be correlated to water holding in plants (Jackson, 1982; Penuelas et al., 1997; Li et al., 2001b; Claudio et al., 2006). The data collected within the measurement grid were grouped by landform for analysis of variance and comparison of means between the shoulder, slope and downslope landform groups. Descriptive statistics and correlation of data were done using PROC UNIVARIATE and PROC CORR procedures (SAS Institute, 1990). The analysis of variance between the landform groups was done using General Linear Models (GLM) procedure. The Honestly Signicant Difference (HSD) was used for comparison of means between the landform groups (SAS Institute, 1990). Variance homogeneity of datasets was veried using the Bartlett test, and normality and residual distribution of data sets were conrmed using PROC UNIVARIATE (SAS Institute, 1990). All variables were mapped with Inverse Distance Weighting (IDW) interpolation using ArcMap 9.1 (Environmental Systems Research Institute Inc., Redlands, CA). 3. Results 3.1. Distribution patterns of solar irradiance, soil water and strawberry water index The descriptive statistics showed that physical properties (site elevation, IRR and SWC), soil pH, and strawberry plant physiological variables (reectance WI, leaf chlorophyll SPAD readings and NDVI) were highly variable (Table 1). The eld topography featured a linear decline from the shoulder, slope to downslope terrain (Table 1) and the interpolated topographic patterns showed the aspect direction and the landform zones (Fig. 1A). The site elevation had a range of 6.3 m with a mean of 2 m difference between the sequent landforms (n = 14 each landform group) and the difference was signicant (P < 0.001, Table 1). The IRR showed the similar patterns as the elevation (Fig. 1B) with values being the highest (830840 W m2 ) in the shoulder area (Table 1), and the difference in IRR was signicantly between the three landforms (P < 0.001, Table 1). The landform had a signicant effect on irradiance (F = 118.68, P < 0.001, df = 2). The honestly signicant difference (HSD) values were 0.9 m for the elevation and 18 W m2 for the IRR variable ( = 0.05). Soil water content (SWC) varied between 0.06 and 0.20 g g1 and the difference in SWC was signicant between the landforms (F = 4.13, P < 0.05, df = 2). The HSD value was 0.03 g g1 for the SWC variable ( = 0.05). The interpolated SWC patterns were spatially dividing by landform (Fig. 1C). Soil pH (mean 6.626.84) was with in the optimal range for strawberry growth. Slightly higher soil pH values were measured in the high radiation shoulder area but the difference was not signicant between the landforms (Table 1). Strawberry plant water index was signicantly higher (WI range 0.640.80) in the slope area than in the shoulder and downslope areas (Table 1). Signicantly higher WI values were situated in the shoulder and slope areas (Fig. 1D). Higher WI indicated a higher plant water stress. As a result, the SPAD readings and the NDVI index values were signicantly lower in the slope areas than in the shoulder and downslope areas. Overall, the datasets were not skewed (kurtosis < 3) except the soil pH in the slope (kurtosis = 3.76) and downslope areas (kurtosis = 4.68) and the sample variances were proportional to the means of variables (Table 1). The HSD values were 0.05 for the WI and 0.04 for the NDVI variable ( = 0.05). The correlations between these physical variables were significant (IRR vs. elevation, r = 0.83, P < 0.01; SWC vs. IRR, r = 0.38, P < 0.05; and SWC vs. elevation, r = 0.36, P < 0.05). These correlation relationships revealed that low SWC was associated with high IRR and high elevation, indicating a water loss possibly from runoff in high elevation shoulder and slope areas.

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Table 1 Descriptive statistics and comparison of site elevation, solar irradiance (IRR), soil water content (SWC), soil pH, strawberry plant reectance water index (WI), leaf chlorophyll concentration (SPAD readings) and plant normalized difference vegetative index (NDVI) in different landform groups at the study site (n = 14 in each landform group). Landform groups Shoulder Mean Standard deviation Sample variance Kurtosis Skewness Minimum Maximum Slope Mean Standard deviation Sample variance Kurtosis Skewness Minimum Maximum Downslope Mean Standard deviation Sample variance Kurtosis Skewness Minimum Maximum Contrasts (F-value inter landform)b Shoulder vs. slope and downslope Slope vs. downslope
a b

Elevationa 21.5 0.6 0.3 0.5 0.3 20.6 22.6 19.5 1.2 1.4 0.8 0.2 17.3 21.3 17.6 0.9 0.7 0.3 0.4 16.3 19.3 118.01** 33.39**

IRRa 820 16.4 270 0.04 0.43 785 844 779 25.6 657.0 1.4 0.1 738 816 709 26.5 701 0.1 0.5 669 765 205.68** 31.67**

SWCa 0.13 0.04 0.11 0.06 0.43 0.06 0.20 0.12 0.06 0.13 0.39 0.40 0.06 0.18 0.16 0.03 0.09 0.98 0.36 0.09 0.20 3.92* 3.76*

pH 6.84 0.50 0.25 1.32 0.86 5.62 7.55 6.71 0.41 0.17 3.76 1.63 5.58 7.25 6.62 0.47 0.22 4.68 1.72 5.30 7.20 0.95 ns 1.44 ns

WI 0.66 0.10 0.21 1.35 0.04 0.61 0.70 0.71 0.13 0.36 0.15 0.07 0.64 0.80 0.52 0.09 0.17 1.19 0.10 0.48 0.57 185.61** 91.68**

SPAD 34.5 4.28 18.4 1.44 0.15 27.5 40.0 30.8 2.43 5.90 1.08 1.32 27.8 35.9 38.6 4.52 20.4 0.89 0.03 32.0 46.2 20.32** 25.84**

NDVI 0.69 0.12 0.17 0.86 0.36 0.65 0.75 0.64 0.16 0.20 0.25 0.26 0.56 0.71 0.81 0.11 0.14 1.44 0.11 0.75 0.87 146** 74**

Elevation in m, IRR in W m2 and SWC in g g1 . ns, * and **: not signicant and signicant at P < 0.05 and at P < 0.001, respectively.

3.2. Trends of strawberry fruit, leaf and soil temperatures Mean day-time air and surface soil temperatures ranged 922 C during the growing season. Maximum air temperatures varied between 26 and 32.4 C during the rst two weeks of July each year. The surface soil temperatures measured in the warmest month (July) were signicantly higher (35.6 0.7 C, range 35.637.4 C) in the shoulder area than in the downslope areas (31.3 0.8 C, range 31.233.0 C). The landform had a signicant effect on the surface soil temperatures (F = 94.75, P < 0.001, df = 2). Soil temperatures were signicantly different between the shoulder, slope and downslope (P < 0.001) and their HSD value ( = 0.05) was 0.98 C (Fig. 2).

The temperatures in July were important because it was the time during the strawberry fruit bulking and maturity period. The temperatures measured on the strawberry fruits and leaves were signicantly different with the HSD value ( = 0.05) of 1.09 C (Fig. 3). Across the nested grid, strawberry surface fruit temperatures varied between 32.9 1.3 C, which was on average 5.8 C higher than leaf temperatures (27.1 0.5 C). The landform had a signicant effect on the fruit, leaf and soil temperatures (F = 135.97, P < 0.001, df = 2). 3.3. Trends of strawberry plant canopy reectance and spectral index During strawberry fruit bulking and maturity period, the canopy reectance was the highest at the NIR band (center 830 nm) follow-

Fig. 2. Comparison of surface soil temperatures in shoulder, slope and downslope areas. Each bar was the mean and standard deviation of 42 readings at each GPS point, measured during early July 2006 and early 2007. The honestly signicant difference (HSD, Tukey test) value was 0.98 C ( = 0.05).

Fig. 3. Comparison of temperatures in soil, strawberry fruits and leaves. Each bar was the mean and standard deviation of 42 readings at each GPS point, measured during July 2006. The honestly signicant difference (HSD, Tukey test) value was 1.09 C ( = 0.05).

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Table 2 Descriptive statistics of strawberry plant reectance in different bands, the ratio vegetative index (RVI), relative nitrogen vegetative index (RNVI), normalized difference vegetative index (NDVI) and reectance water index (WI). n = 42. 485 nma Mean Standard deviation Sample variance Kurtosis Skewness Minimum Maximum CV (%)
a

560 nma 9.77 1.24 1.53 0.07 0.23 6.83 13.62 13

660 nma 8.62 2.23 4.97 0.28 0.35 4.10 15.13 26

830 nma 51.3 3.19 10.2 0.01 0.07 43.3 60.9 6

1650 nma 31.9 2.55 6.50 0.23 0.23 26.3 39.9 8

RVI 6.45 2.07 4.28 0.93 1.02 3.18 13.9 32

RNVI 5.36 0.90 0.82 0.56 0.72 3.55 8.32 17

NDVI 0.71 0.07 0.01 0.45 0.20 0.52 0.87 10

WI 0.63 0.07 0.01 0.57 0.17 0.48 0.80 12

4.89 1.06 1.13 0.16 0.43 2.67 8.05 22

Reectance data are in %.

ing the water band (center 1650 nm) (Table 2), as plants absorbed strongly visible energy and reected NIR energy. The descriptive statistics showed that all the reectance data and spectral index values were not skewed (small kurtosis values 0.071.02, Table 2). The NIR reectance was signicantly lower in the slope area (mean 46%) compared to in the downslope at terrain (mean 54%). The green band reectance was slightly higher than the red band. As a result, the ratio vegetative index (RVI) was higher than the relative nitrogen vegetative index (RNVI). The NDVI and reectance WI values were compatible (Table 2). Similar to the NDVI distributions pattern (Table 1), the high RVI (12.113.9) and high RNVI values (7.18.3) were measured in the downslope areas. The landform had the signicant effects on the blue (F = 61.9, P < 0.001, df = 2), green (F = 44.0, P < 0.001, df = 2), red (F = 62.07, P < 0.001, df = 2), NIR (F = 52.32, P < 0.001, df = 2) and the MIR reectance (F = 55.8, P < 0.001, df = 2). There were also signicant landform effects on the spectral index RVI (F = 56.9, P < 0.001, df = 2) and RNVI (F = 62.3, P < 0.001, df = 2). The HSD values were 1.4 for the RVI and 0.52 for the RNVI variable ( = 0.05). All reectance variables and spectral index were signicantly correlated (Table 3). The NIR reectance was negatively correlated with the visible and MIR reectance but positively correlated with the RVI and RNVI (Table 3).

reectance data (Table 3). There were similarly signicant correlations for the SPAD and the spectral variables (Table 3), as a result of the comparable patterns for the leaf chlorophyll and yield variables. Strawberry marketable yield was negatively related to IRR (R2 = 0.32, P < 0.05, Fig. 5A), reectance WI (R2 = 0.41, P < 0.05, Fig. 5B), and site elevation (R2 = 0.45, P < 0.05, Fig. 5C) but positively correlated with SWC (R2 = 0.45, P < 0.05, Fig. 5D). In contrast, strawberry marketable yield was positively related to the canopy spectral reectance indexes and leaf chlorophyll including NDVI, RNVI, RVI and SPAD leaf chlorophyll readings (0.46 < R2 < 0.68, P < 0.05, Fig. 6). The distribution patterns of strawberry leaf chlorophyll SPAD readings against the physical variables (solar irradiance, reectance water index, soil water content (SWC), and site elevation (SE) and the strawberry canopy spectral reectance indexes (NDVI and RNVI) were similar to the strawberry yield patterns (Figs. 5 and 6). The correlations between these variables (n = 42) could be described by the linearly regression equations as follows: SPAD = 78.56SWC + 24.26, SPAD = 1.7408SE + 59.84, NDVI = 0.0097SPAD + 0.3767, RNVI = 2.2215SPAD + 22.68, R2 = 0.40, P < 0.05 R2 = 0.47, P < 0.05 R2 = 0.38, P < 0.05 R2 = 0.35, P < 0.05

3.4. Relationships of strawberry fruit sets, canopy reectance, solar irradiance and soil water The strawberry fruit sets were tenser in the downslope areas than in the shoulder area and fruit sets and fruit sizes were reduced on the slope. As a result, strawberry total fruit yield were significantly different between the three position areas (Fig. 4A). The strawberry total fruit yield decreased from 1.88 0.37 kg m2 in the shoulder area to 1.36 0.22 kg m2 in the slope. With low solar irradiance and high water content, the strawberry total fruit yield increased to 2.65 0.53 kg m2 in the downslope area, which meant that water and irradiance were critical for this small fruit bearing. The fruit sizes were also larger in the higher SWC soil in the down-at area, as the marketable fruit yields (fruit sizes 2.5 cm) were 81.5%, 72.9% and 69.1% of the total yields in the downslope, slope and shoulder areas, respectively. The strawberry marketable fruit yields were signicantly higher (2.16 0.66 kg m2 ) in the downslope area (Fig. 4B). The landform had the signicant effects on the strawberry total yield (F = 32.34, P < 0.001, df = 2) and marketable yield (F = 21.52, P < 0.001, df = 2). The HSD values were 0.4 kg m2 for the total yield and 0.47 kg m2 for the marketable yield variable ( = 0.05, Fig. 4). Strawberry fruit yield also had the highest variations among the measured variables, with a high coefcient of variation (CV = 46%). The interpolated patterns for the strawberry marketable yields were comparable to the leaf chlorophyll (Fig. 1EF). The strawberry fruit yield was positively correlated with NIR reectance and spectral index RVI and RNVI and negatively correlated to visible and MIR

4. Discussion 4.1. Strawberry plant irradiance, temperature and water stress Strawberry plants are perennial, growing in the eld during hot and cold seasons and strawberry is adapted to the environment with temperature variations (Heide, 1977). Grown in the shallow, gravel soil, the variation in strawberry fruit yield and plant physiological variables (chlorophyll and reectance measurements) revealed that in landscapes with topographic inuences, solar irradiance, temperatures and SWC had signicant effects on strawberry fruiting ability, as shown their relationships with the strawberry fruit yield (Figs. 5 and 6). It was reported that the correlations between solar irradiance, temperature and elevation were positively signicant (Rorison et al., 1986; Florinsky et al., 1994). The role of topography was attributed to its inuence on the thermal and hydrologic processes inuencing the strawberry plant vigor and its fruit bearing efciency (yield). Strawberry plant water stress (WI values > 0.6) occurred on the slope and shoulder areas, where there was high irradiance (Table 1) and temperature (Fig. 2) and low SWC values (Table 1), resulting in signicantly lower fruit yield (Fig. 4). The negative regression relationship between strawberry yield and solar irradiance (Fig. 5) further suggested that the inuence of soil water in strawberry growth seemed to be complicated by solar irradiance and site ele-

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Table 3 Pearson correlation coefcients (r) of strawberry marketable fruit yield plant reectance in different bands, the ratio vegetative index (RVI), relative nitrogen vegetative index (RNVI), normalized difference vegetative index (NDVI) and reectance water index (WI). n = 42. Yield Yield SPAD 485 nm 560 nm 660 nm 830 nm 1650 nm RVI RNVI 1 0.78** 0.69* 0.62* 0.68* 0.71** 0.66* 0.69* 0.68* SPAD 1 0.58* 0.48 ns 0.56* 0.57* 0.59* 0.51* 0.50* 485 nm 560 nm 660 nm 830 nm 1650 nm RVI RNVI

1 0.97** 0.99** 0.82** 0.93** 0.95** 0.95**

1 0.97** 0.74** 0.91** 0.94** 0.95**

1 0.81** 0.93** 0.95** 0.95**

1 0.69* 0.86** 0.88**

1 0.87** 0.86**

1 0.99**

: ns, * and **: not signicant and signicant at P < 0.05 and at P < 0.01, respectively.

Fig. 4. Comparison of strawberry total fruit yield (A) and marketable fruit yield (B) measured in the shoulder, slope and down at areas, respectively. Each bar was the mean and standard deviation of 14 measurements in a 1-m2 area. The honestly signicant difference (HSD, Tukey test) values were 0.40 kg m2 for the total yield and 0.47 kg m2 for the marketable yield variables ( = 0.05).

vation because of high radiation and water runoff in high position areas (Fig. 5). Supra-optimal temperature (2426 C) exerted a modifying inuence on the response of strawberry and at 30 C the plants failed to form the ower buds (Ito and Saito, 1962; Heide, 1977). High temperatures associated with drought could also induce the

earlier ower bud formation (Klamkowski and Treder, 2008). Temperature or soil water status associated with topographic features could further affect soil nutrient distribution, and thus crop nutrient uptake and yields (Rorison et al., 1986; Li et al., 2001b, 2002), which would explain the variation of strawberry yield (Fig. 4) and its correlation with the plant nitrogen status (NDVI and RNVI) and

Fig. 5. Regression relationships of strawberry marketable fruit yield and solar irradiance (IRR in W m2 , (A); strawberry marketable fruit yield and reectance water index (WI, B); strawberry marketable fruit yield and site elevation (SE in m, C); and strawberry marketable fruit yield and soil water content (SWC in g g1 , D).

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Fig. 6. Regression relationships of strawberry marketable fruit yield vs. normalized difference vegetative index (NDVI, A); strawberry marketable fruit yield vs. relative nitrogen vegetative index (RNVI, B); strawberry marketable fruit yield vs. ratio vegetative index (RVI, C); and strawberry marketable fruit yield vs. leaf chlorophyll SPAD readings (D).

leaf chlorophyll content (Fig. 6). The similar approach has been used for quantifying plant abiotic stress (Carter and Knapp, 2001). Strawberry fruit surface temperatures were slightly higher than leaves (Fig. 3), which would be due to the heat accumulation in the fruits. The lack of correlation between soil pH and strawberry yield and other measured variables would be because there was no difference in soil pH within the eld (Table 1). The decline in strawberry fruit yields in slope and shoulder areas could also be the consequence of high IRR and water decit stress leading to reduced leaf stomatal activity, water channel activity in stolons and distribution of photoassimilates within strawberry plants associated with drought stress, as comparable to the consequences reported in other studies (Blanke and Cooke, 2004; Klamkowski and Treder, 2008). The water decit in the shoulder and slope areas was shown by their signicantly higher WI (0.750.82) compared to the WI values (0.480.65) in the downslope terrain. Plant water stress occurred when the plant demand for water exceeded the available amount during a certain period and water stress was among the principal causes of reduced plant development and reduction in crop yield (Grifths and Parry, 2002; Claudio et al., 2006; Li et al., 2008). Plant water stress could lead to stunted growth, and water-stressed strawberry plants might not enable for vigorous fruit bearing. The ability to recognize early symptoms of plant water stress was crucial without signicant economic reduction of crop yield (Blum, 1996; Grifths and Parry, 2002). The WI index and canopy infrared temperature could be a real-time indicator of plant water stress minimizing negative impacts of water decit on plant growth and development (Jackson, 1982; Penuelas et al., 1997; Claudio et al., 2006). 4.2. Strawberry plant water holding and plant vigor related to reectance and spectral index Strawberry plant water holding status could also be explained using the reectance WI, estimated using the water band MIR

reectance to the NIR reectance. High WI value meant low water holding in the plants. The WI was a useful estimate of yield loss from plant water stress as its regression relation with the strawberry fruit yield was signicant (Fig. 5B). The MIR band (center 1650 nm) was within the two major water bands (1400 and 1900 nm), the NIR (center 830 nm) was away the water bands, and therefore the correlation between NIR and MIR reectance was signicantly negative (Table 3). This relation conrmed that the use of NIR band was adequate for determination of plant water holding, as shown in Claudio et al. (2006). As the MIR reectance was positively correlated with the blue, green and red bands (0.91 < r < 0.93, Table 3), it indicated when the strawberry plant reected more visible and MIR energy, the plants were more water stressed. High MIR reectance meant low water content in the plants. Plants containing less water would reect more MIR band energy than plants containing higher water content (Jackson, 1982; Li et al., 2001a). When the SWC was low, plants had to use more energy to uptake available water and nutrients, and plants might develop stress symptoms (Sperry et al., 2002; Li et al., 2008). Low NIR reectance would mean a small leaf area and small plant ground cover (Jackson, 1982; Carter and Knapp, 2001; Li et al., 2001a). The high reection of NIR energy corresponding to the high absorption of MIR energy and high leaf chlorophyll of strawberry plants (Table 3) would mean a strong plant vigor. Leaf chlorophyll molecule was vital for photosynthesis that could absorb the sunlight to help plants get energy from lights, and leaf chlorophyll was commonly considered as indicator of plant growth status (Markwell et al., 1995). Plant water stress status and plant ecophysiological processes could be detected from color, vigor, and morphology of stressed plants (Li et al., 2001a; Claudio et al., 2006). Also, a physiological approach to understand how plants could adapt to water decit in the soil would be measuring their multispectral reectance, i.e., a ratio of incoming to outgoing radiation in the visible and near infrared bands and its canopy infrared temperature (Jackson, 1982; Li et al., 2001b).

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4.3. Planting design and orientation of rows for light and water management Full sunlight exposure through the canopies is a key factor for maximizing fruit bearing (Heide, 1977; Watson et al., 2002; Rieger, 2005). The consequences of uneven landforms and internal drainage constraints from the current study included uneven distribution of light spectrum (Table 1), temperatures (Fig. 1) and soil water (Table 1) and insufcient strawberry plant water holding (high WI) and low fruit bearing in slope areas (Fig. 4). As most elds commonly characterize by uneven landforms, each crop has a specic minimum threshold growth and water requirement for economic production in a given environment. Evaluation of whole plant responses to a given water shortage is difcult because of many other factors also affecting the production system (Blum, 1996; Grifths and Parry, 2002; Sperry et al., 2002). New planting designs which consider an alternative orientation of rows can be an option for improving light and water management in this soil having natural rolling and internal drainage constraints. The current orientation of rows following the aspect direction (NS) is useful for sunlight exposure to the strawberry plants and water drainage in case of heavy rainfall. Being in the humid Atlantic coast, there is excess precipitation in the region (mean annual rainfall 1200 mm and high rainfall frequency in the spring). Therefore in farming practices row orientation for fruit crop planting is usually along the aspect to support drainage in the spring and to help increase soil temperature during that time of year. However, as rainfall is reduced in the summer and strawberry plants requires more water during the full vegetative stage for ower bud formation and fruit bearing, the row orientation along the aspect seems not to help for reducing water runoff and internal drainage. It is suggested that alternative orientation of row in the NESW direction or the WE direction would help reduce both water losses from surface runoff and internal drainage during the important strawberry owering and fruiting period. Also, as the strawberry is planted on the raised beds, the soil can warm up sooner in the spring and the canopies can still be fully exposed to sunlight with the NESW or WE orientation of rows. Other options for water management in this soil with natural runoff and internal drainage constraints would be introducing drip irrigation. Sprinkle irrigation is useful for frost protection but drip irrigation is more efcient than overhead irrigation in terms of plant water use. Drip irrigation reduces water runoff and requires 50% less water (El-farhan and Pritts, 1997). Also, water management could include establishing runoff control systems by adding organic matter which can be mixed into the soil for sealing the surface to reduce inltration (Li et al., 2004). Future study on light and water management for naturally undulating conditions with rapid internal drainage constraints would be evaluated using new planting design with alternative orientation of rows for capturing maximum sunlight interception and reducing water runoff, especially during fruit bearing period. In this coast area, growers have practiced strawberry rotations with ryegrass for reducing tillage for soil and water conservation. Other practices have included keeping soil in place by planning a cover crop for soil protection. More information such as adding organic matter into the soil to reduce inltration and strawberry owering and budding capacity in relation to early season temperature, irradiance and water availability is needed for developing management strategies for enhancing high-value horticultural crop production in the soils with these natural constraints. 5. Conclusions Lights and water were not evenly distributed in the eld with topographic features and rapid internal drainage constraints.

Solar radiation, temperature and mainly water availability were factors associated with site elevation to inuence strawberry fruiting efciency. Strawberry fruit yield were negatively correlated with solar irradiance, which suggested that high solar radiation and high temperature associated with water loss would exert a signal negative inuence on the responses of cool-weather strawberry plants and consequently reducing fruit formation. Strawberry plants in the slope areas were more water stressed with a higher reectance WI, and therefore reduced fruiting rates. Strawberry plant vigor, expressed by leaf temperature, whole plant multispectral reectance, and WI, NDVI, RNVI and RVI determined from whole plant multispectral signals could be real-time indicators of plant light and water conditions. It is suggested that NS orientation of rows following the aspect may create water stress conditions during fruit bearing period. A new planting design for alternative orientation of rows and drip irrigation would be tested for capturing maximum sunlight and reducing water loss in the elds with natural constraints. Acknowledgements We thank Nova Scotia Department of Agriculture (NSDA) Technology Development Program, Advancing Canadian Agriculture and Agri-Food Council Agri-Futures Program, Horticulture Nova Scotia, Millen Farms, and National Natural Science Foundation of China (NSFC, Project 40671110/D0115) for support for this study. References
Blanke, M.M., Cooke, D.T., 2004. Effects of ooding and drought on stomatal activity, transpiration, photosynthesis, water potential and water channel activity in strawberry stolons and leaves. Plant Growth Reg. 42, 153160. Blum, A., 1996. Crop responses to drought and the interpretation of adaptation. Plant Growth Reg. 20, 135148. Carter, G.A., Knapp, A.K., 2001. Leaf optical properties in higher plants: linking spectral characteristics to stress and chlorophyll concentration. Am. J. Bot. 88, 677684. Claudio, H.C., Cheng, Y., Fuentes, D.A., Camon, J.A., Luo, H., Ocechel, W., Qiu, H.L., Rahman, A.F., Sims, D.A., 2006. Monitoring drought effects on vegetation water content and uxes in chaparral with the 970 nm water band index. Rem. Sens. Environ. 103, 304311. Cole, R.G., Healy, T.R., Wood, M.L., Foster, D.M., 2001. Statistical analysis of spatial pattern: a comparison of grid and hierarchical sampling approaches. Environ. Monit. Assess. 69, 8599. El-farhan, A.H., Pritts, M.P., 1997. Water requirements and water stress in strawberry. Adv. Strawb. Res. 16, 512. Florinsky, I.V., Kulagina, T.B., Meshalkina, L., 1994. Inuence of topography on landscape radiation temperature distribution. Int. J. Rem. Sens. 15, 31473153. Grifths, H., Parry, M.A.J., 2002. Plant responses to water stress. Ann. Bot. 89, 8011801. Ganmore-Neumann, R., Kafka, U., 1985. The effect of root temperature and nitrate/ammonium ratio on strawberry plants. II. Nitrogen uptake, mineral ions, and carboxylate concentrations. Agron. J. 77, 835840. Heide, O.M., 1977. Photoperiod and temperature interactions in growth and owering of strawberry. Physiol. Plantar. 40, 2126. Hetherington, A.M., Woodward, F.I., 2003. The role of stomata in sensing and driving environmental changes. Nature 424, 901908. Ito, H., Saito, T., 1962. Studies on the ower formation in the strawberry plants. 1. Effects of temperature and photoperiod on the ower formation. Tohoku J. Agric. Res. 13, 191203. Jackson, R.D., 1982. Canopy temperature and crop water stress. Adv. Irrig. 1, 4385. Keutgen, A.J., Pawelzik, E., 2009. Impacts of NaCl stress on plant growth and mineral nutrient assimilation in two cultivars of strawberry. Environ. Exp. Bot. 65, 170176. Klamkowski, K., Treder, W., 2008. Response to drought stress of three strawberry cultivars grown under greenhouse conditions. J. Fruit Ornam. Plant Res. 16, 179188. Li, H., Lascano, R.J., Barnes, E., Booker, J., Wilson, L.T., Bronson, K.F., Segarra, E., 2001a. Multispectral reectance of cotton related to plant growth, soil water, texture, and site elevation. Agron. J. 93, 13271337. Li, H., Lascano, R.J., Wilson, L.T., Segarra, E., 2001b. Semivariance and crosscorrelation of cotton canopy temperature, plant reectance, and soil properties in the landscape. In: Blackmore, S., Grenier, G., (Eds.), Precision Agriculture. Montpellier, France, pp. 241246. Li, H., Lascano, R.J., Booker, J., Wilson, L.T., Bronson, K.F., Segarra, E., 2002. State-space description of eld heterogeneity: water and nitrogen use in cotton. Soil Sci. Soc. Am. J. 66, 585595.

174

H. Li et al. / Environmental and Experimental Botany 68 (2010) 165174 Rorison, I.H., Sutton, F., Hunt, R., 1986. Local climate, topography and plant growth in Lathkill Dale NNR. 1. A twelve-year summary of solar radiation and temperature. Plant Cell Environ. 9, 4956. SAS Institute, 1990. SAS/STAT users guide, vol. 2, GLM-VARCOMP. Version. 6, 4th ed. SAS Institute. Cary, NC. Shah, N.H., Paulsen, G.M., 2003. Interaction of drought and high temperature on photosynthesis and grain-lling of wheat. Plant Soil 257, 219226. Sperry, J.S., Hacke, U.G., Oren, R., Comstock, J.P., 2002. Water decits and hydraulic limits to leaf water supply. Plant Cell Environ. 25, 251263. Wang, S.Y., Lin, H.S., 2006. Effect of plant growth temperature on membrane lipids in strawberry. Sci. Hort. 108, 3542. Watkins, C.A., McNicol, R.J., Young, K., Jones, A.T., 1990. The effect of heat treatment and meristem-tip culture on June Yellows in strawberry. Ann. Appl. Biol. 116, 489492. Watson, R., Wright, C.J., McBurney, T., Toylor, A.J., Linforth, R.S.T., 2002. Inuence of harvest date and light integral on the development of strawberry avour compounds. J. Exp. Bot. 53, 21212129. Webb, K.T., Thornpson, K.L., Beke, G.J., Norvland, J.L., 1991. Soils of Colchster County, Nova Scotia. Report No. 19, Nova Scotia Soil Survey. Research Branch, Agriculture and Agri-Food Canada. Ottawa, ON, p. 201.

Li, H., Parent, L.E., Karam, A., Tremblay, C., 2004. Potential of Sphagnum peat for improving soil organic matter pool, water holding capacity, bulk density and potato yield in a sandy soil. Plant Soil 265, 353363. Li, H., Payne, W.A., Michels, J., Rush, C.M., 2008. Reducing plant abiotic and biotic stress from drought and attacks of greenbugs, corn leaf aphids and virus disease in dryland sorghum. Environ. Exp. Bot. 63, 305316. Markwell, J., Osterman, J.C., Mitchell, J.L., 1995. Calibration of the Minolta SPAD-502 leaf chlorophyll meter. Photosyn. Res. 46, 467472. Marriott, C.A., Hudson, G., Hamilton, D., Neilson, R., Boag, B., Handley, L.L., Wishart, J., Scrimgeour, C.M., Robinson, D., 1997. Spatial variability of soil total C and N and their stable isotopes in an upland Scottish grassland. Plant Soil 196, 151162. Penuelas, J., Pinol, J., Ogaya, R., Filella, I., 1997. Estimation of plant water concentration by the reectance water index WI (R900/R970). Int. J. Rem. Sens. 18, 28692875. Rieger, M., 2005. In: Rieger, M. (Ed.), Strawberry. Introduction to Fruit Crops. Haworth Food & Agricultural Products Press, New York, pp. 383392. Robert, F., Risser, G., Petel, G., 1999. Photoperiod and temperature effect on growth of strawberry plant (Fragaria ananassa Duch.): development of a morphological test to assess the dormancy induction. Sci. Hort. 82, 217226.