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Effect of sowing date on rates of leaf appearance, final leaf numbers and areas in Brassica campestris, B. juncea, B. napus and B. carinata
i
ELSEVIER
Field Crops Research 42 (1995) 125-134
Field Crops Research
Effect of sowing date on rates of leaf appearance, final leaf numbers and areas in Brassica campestris, B. juncea, B. napus and B. carinata R. Nanda a, S.C. Bhargava a, H.M. Rawson b,. ~Division of Plant Physiology, Indian Agricultural Research Institute, New Delhi-llO 012, India b Division of Plant Industry, CSIRO, GPO Box 1600, Canberra, A.C.T. 2601, Australia
Received 26 July 1994; accepted 13 May 1995
Abstract B. campestris (cv. Pusa Kalyani), B.juncea (cv. Varuna), B. napus (cv. BO 706) and B. carinata (cv. Tall-1 ) were studied in the field at five dates of sowing during one cropping season. Photoperiod at the successive sowing dates declined from 11.310.2 h and mean temperature from 24 to 15°C. Planting date had a big effect on the duration to the appearance of the first leaf with the range being from 10.8 (sowing 1) to 22 days after sowing (sowing 5), equivalent to a delay of 1.35 days for each I°C reduction in mean temperature. Base temperatures for this phase were approximately 5°C for all species. Planting date had no significant effect on the rate of appearance of subsequent leaves which ranged between 2.68 (date 1) and 2.84 days per leaf (date 3) and averaged equivalent to 0.37 + 0.003 leaves per day. However, rates of leaf appearance differed over a 35% range amongst species, with new leaves appearing every 2.33 _ 0.07 days (B. campestris), 2.71 + 0.12 (B. juncea), 2.90_+ 0.09 (B. carinata), and 3.18 + 0.08 days (B. napus). Upper leaves emerged between 33 and 48% faster than lower leaves depending on species, and this was most apparent at the final two sowings, and particularly in B. napus. Final leaf number declined with later sowing at a rate ranging between 0.186 (B. campestris) and 0.112 leaves per day (B. juncea). Absolute numbers differed amongst species from 35 (B. carinata, sowing 1) to 12 (B. campestris, sowing 5), but were positively correlated with days from sowing to floral initiation. Area per leaf increased with leaf position reaching a peak in the leaf that was emerging at approximately the time of floral initiation with B. napus leaves on average increasing fastest ( 100 cm2 per leaf position) and B. carinata slowest (60 cm2 per leaf). Planting date affected areas of individual leaves largely through changing the timing of floral initiation and by consequence the degree of advancement of the leaf area profiles. It is concluded that although some of the leaf number and area characteristics are under the control ofphenological development, there is considerable variation amongst species aside from this. Keywords: Brassica; Date of sowing;Leaf area; Leaf number;Managementpractices; Phenology
1. Introduction Leaf area per unit ground area determines the percentage of solar radiation intercepted by a crop and * Correspondingauthor. 0378-4290/95/$09.50 © 1995 ElsevierScienceB.V. All rights reserved S S D I 0 3 7 8 - 4 2 9 0 ( 9 5 ) 00026-7
therefore has a predominant influence on crop growth (Watson, 1956; Sinclair, 1984). The rate of establishment of leaf area after sowing is particularly important to subsequent crop growth (Gallagher, 1979). Thurling (1974) and Clarke and Simpson (1978) con-
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R. Nanda et al. / Field Crops Research 42 (1995) 125-134
cluded that in summer rape, seed yield and maximum leaf area index are positively correlated and similar conclusions have been reached for irrigated sunflower (Rawson and Turner, 1983). Though these correlative observations have been made, there are few comparative studies of several Brassica species in the field to establish whether there are differences amongst species in their rates of leaf area establishment, their final leaf areas, and particularly the means by which they achieve their final leaf numbers and areas. Furthermore, there are few field studies which have attempted to examine how environmental factors may change the parameters of leaf area production. To quantify leaf development in soybean (Glycine max. L.), Hofstra et al. (1977) described it in terms of leaf appearance rate, leaf area expansion rate, maximum leaf area and leaf area duration. A similar analytical approach in Brassica species would demonstrate whether there are differences in these parameters among species and even whether there might be scope for inter-species hybridisation to improve the rate of crop leaf area development. It is likely that environmental variables will change these parameters as occurs in sunflower (e.g. Rawson and Dunstone, 1986), and possibly even change them differentially amongst the species. For example, one of those environmental variables, temperature, affects many plant processes and especially plant development (Coelho and Dale, 1980; Slafer and Rawson, 1994), and has been shown in wheat to affect cultivars differentially in phenological development and leaf emergence (Slafer and Rawson, 1995). Consequently, in any study of development it
is important to establish whether the parameters of interest are changed by the environment, and if so, to what degree. The present study describes the changes that occur in several parameters of leaf area production when planting date is changed in the field and compares four Brassica species for their responses.
2. Material and methods
Four species of Brassica, B. campestris cv. Pusa Kalyani; B. juncea cv. Varuna, B. napus cv. BO-706 and B. carinata cv. Tall-1 were planted at intervals during the cropping season of 1991-92. Sowings were on 19 and 29 October, 8 and 28 November, and 9 December, in 5 × 4 m plots with 45 × 20 cm spacing thus giving 12 plants m -2. N, P and K at 40:40:40 kg h a - ] was applied before sowing. After germination, six plants in 1 m row length in each treatment were selected for observations. All leaves on these plants were tagged and numbered in sequence from the base to the top of the plant when they were about 1 cm long. Leaf length and breadth were measured at the widest point of the blade every second or third day until maximum length was reached and final area was estimated for each leaf from the product of maximum length and breadth. Detailed observations were taken on 15 leaves in early cultivars and 20 leaves in late-maturing cultivars. Rates and durations of leaf area expansion was estimated by fitting second-order polynominal equations to the data of area by time in days for each leaf.
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R. Nanda et al. / Field Crops Research 42 (1995) 125-134
Records of daily maximum and minimum temperature (Fig. la) were obtained from the Indian Agricultural Research Institute Meteorological Station located less than 100 m away from the experimental site. Degree days with units of °Cd were calculated by accumulating the mean of these maximum and minimum temperatures above a base temperature of 0°C. The °Cd sums were accumulated independently for each leaf or each growth stage. Assuming a critical light intensity of 15 lux for photoperiodic response of wheat (Gotch, 1977), it was determined graphically that this requirement would be met when the sun is at an elevation of more than -3053 '. Daily values of photoperiodic day-length were therefore taken as the duration of the day when angle exceeded this value following Robertson and Russel (1968). The hour values of photoperiod calculated, and the rates in minutes at which photoperiod changed each day are shown on Fig. lb. On the figure, sowing dates were equivalent to days 1, 11, 21, 41, and 52 for the five respective plantings. As can be seen, photoperiod at planting reduced over a relatively narrow range from 11.3 to 10.2 h amongst sowing dates and photoperiods only started to increase some 10 days after the last planting. Mean temperatures at sowing changed from 24 to 15°C.
3. Results
3.1. Leaf emergence Although temperature and photoperiod were changing throughout the study, leaves appeared approximately linearly with time after sowing in all species (Fig. 2a, d, g, j ). Linear regressions fitted between leaf position and time, considering each sowing date and species separately, all had coefficients of determination which were better than r 2 = 0.95. Averaging across species, a new leaf appeared every 2.78 ___0.03 days, with a small range amongst planting dates of from 2.68 (planting 1) to 2.84 days per leaf (planting 3). The overall mean value is equivalent to 0.37 + 0.003 leaves per day (cf. values of 0.35-0.40 leaves/day for summer rape according to Campbell and Kondra (1977)). However, average rates of leaf appearance differed amongst species over a 35% range with new leaves appearing every 2.33+0.07 days (B. campestris),
127
2.71 ___0.12 (B.juncea), 2.90__+ 0.09 (B. carinata), and 3.18-t-0.08 days (B. napus). These results support those of Kasa and Kondra, 1986) who found that B. campestris had a higher leaf emergence rate than B. napus during all growth periods. The main difference between planting dates in the time taken between sowing and the appearance of any leaf was not the slopes or rates of leaf appearance, but the intercepts i.e. when the first leaf appeared after crops were sown. Thus, on average across species, and for the respective sowing dates, leaf 1 appeared on day 10.8+0.31 (sowing 1), 12.6+__1.00 (2), 13.6+__1.06 (3), 18.9+ 1.13 (4), and day 22.0+0.39 (5) after sowing. The day of appearance of leaf 1 was well correlated linearly and inversely with the temperatures between sowing and that day, with no apparent statistical difference in the effect of maximum, mean, or minimum temperatures. Thus, using the mean temperature, the appearance of leaf 1 was delayed by 1.35 days for each 1°C reduction in temperature. Using the same data to calculate the base temperature for time to leaf 1 (i.e. regressing 1/days between sowing and leaf 1 against mean temperature for that period, see Angus et al., 1981), the range was between 4.1 and 5.5°C, depending on which data points were included (cf. 5°C estimated by Morrison et al., 1989 for summer rape grown in western Canada). Base temperatures thus calculated for B. campestris, B. juncea, B. napus, and B. carinata respectively were 5.7, 6.6, 4.6, and 5.3°C. Clearly, there were no marked differences between species in this parameter. We have redrawn the curves of Fig. 2a, d, g, j (after removing from the x-axis the calculated number of days between sowing and leaf 1 emergence), as Fig. 2b, e, h, k, respectively, to see whether most of the variation between sowings in time of leaf appearance is due to differences in time of appearance of the first leaf. Visually this appears to be the case. It also seems to be the case statistically, since if we then fit linear regressions through the combined data sets for each species, we see that the variance ratios ( F values) have increased from 384 to 1275 (Fig. 2a vs 2b, B. campestris), 538 to 1312 (Fig. 2d vs 2e, B.juncea), 87 to 1826 (Fig. 2g vs 2h, B. napus) and from 400 to 2242 (Fig. 2j vs 2k, B. carinata ) . If temperature is the main factor affecting the time between sowing and appearance of leaf 1, as seems to be supported from the above analysis, we might expect
R. Nanda et al. / Field Crops Research 42 (1995) 125-134
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129
R. Nanda et al. / Field Crops Research 42 (1995) 125-134
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Fig. 3. Effect of planting date on rate of change in phyllochron ( + 2 X se) between leaves 1 and 15 (a). Also shown are rate of change of photoperiod (open squares, a) and minimum temperatures (b) for these plantings using mean daily data between sowing and the appearance of leaf 8. Planting dates were 19, 29 October, 8, 28 November and 9 December.
that differences in temperature might be causing any spread of response in the rates of appearance of subsequent leaves. The analysis in Fig. 2c, f, i, and 1, where thermal time (°Cd > 0°C) is substituted for days, does not appear to support that proposition, as F values for linear regressions through the data are smaller than those using only calendar time as the x-axis (respective F values for species were 700, 1183, 1141, and 1925). We have used 0°C as the base temperature in this figure, rather than the 5°C suggested by Morrison et al. (1989), but that will have no effect on the relationships shown. What we have assumed thus far, to keep the analysis simple, is that upper and lower leaves appear at much the same rate. In fact, upper leaves often appeared faster (and so had shorter phyllochrons) than lower leaves and this was particularly true for B. campestris and B. napus for the later sowings. This difference is demonstrated by comparing the linear regressions between leaf position and thermal time averaged across sowings for leaves 1-6 and for 7-15. Thus, for B. campestris, B. juncea, B. napus, and B. carinata, mean phyllochrons (°Cd> 0°C/leaf) for leaves 1-6 were 59.9, 64.9, 82.6 and 63.7°Cd respectively, and for leaves 7-15 were 31.3, 40.7, 45.2 and 42.9°Cd. This shows that there was a reduction in phyllochron associated with higher leaf position in all species. In relative terms the reduction was 48, 37, 45, and 33% for the respective species. Further examination of Fig. 2 indicates that it is the later sowings that show the greatest reduction in phyllochron with sowing date. If we now test this visual assessment by regression, we find that phyllochron is
decreasing on average across species from leaves 1-15 for the five sowing dates by 1.92 i- 0.60, 2.63 4- 0.64, 2.02+0.86, 4.91 +0.49, and 3.28_0.38°Cd per leaf respectively. All species had their greatest reduction with leaf position at sowing 4 with the response by B. napus being greatest and that in B. carinata least. The average pattern is shown in Fig. 3a. Also shown in Fig. 3 is the rate of change of photoperiod at the time of emergence of leaf 7 (see Slafer et al., 1994a, b for a discussion of the importance to phenological development of rate of change of photoperiod) and the mean minimum temperature between sowing and emergence of leaf 7 for sowings 1-5. Minimum temperature may have some impact on accelerating phenology through its effect on satisfying a vernalisation response (see Hodgson, 1978a for responses of B. campestris and B. napus to vernalisation). Clearly there are associations between rate of change of phyllochron and the weather parameters shown in Fig. 3. For example, it would be possible to argue that the considerably more rapid development of upper leaves at sowings 4 and 5 was associated with photoperiods starting to lengthen at that time, and with temperatures reaching values which would accelerate the vernalisation process. Whether the associations are causal cannot be assessed without controlled environment experimentation. However, from the above data on change in phyllochron, we might guess that B. napus is one of the more sensitive species to these parameters. 3.2. Final leaf number We have analysed only the first 15 leaves on each species for rate of appearance, but there were many
130
R. Nanda et al. / Field Crops Research 42 (1995) 125-134 40
3.3. Leaf area
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more leaves produced particularly in the later lines B. napus and B. carinata. These were all counted to show that final leaf number also changed with sowing date, with a universal reduction in number with later planting under lengthening photoperiods and lower temperatures (Fig. 4). The rate of reduction with sowing date was the same in B. napus and B. carinata (0.167 and 0.168 leaves per day for days after 19 October, r 2 = 0.93 and 0.97) with a 33% lower slope in B. juncea ( - 0 . 1 1 2 leaves day -~, P = 0 . 9 8 4 ) and a slightly greater slope in B. campestris ( - 0.186 leaves day- ~, P = 0 . 9 9 1 ) . However, the much greater differences between the species than the rates of change with sowing date, were the calculated intercepts at the first sowing of 20.6, 18.2, 26 and 35.2 leaves for B. campestris, B. juncea, B. napus, and B. carinata respectively. This indicates that the absolute responses to the changing environment (cold and photoperiod) in terms of leaf number differed only marginally between species, but that the environmental parameters determining basal leaf number must differ substantially between species. The environmental parameters determining final leaf number are most likely to be those which step the plant through from primarily vegetative, to primarily floral development i.e. that determine phenological development. This notion is given support in Fig. 5 which shows the significant linear correlation between the final number of leaves (y) for each species and the number of days each species takes from sowing to floral initiation (x). The species which flowered early also had few leaves.
All four species followed the pattern of leaf area vs leaf position shown by dicots with an apical meristem which expands laterally with age (cf. Moncur, 1981, and see the similarities with sunflower in Rawson and Dunstone, 1986). Thus, in general, area per leaf increased with successive leaves (Fig. 6a), reaching a peak in three of the species in the leaf that was emerging at approximately the time of floral initiation ( see later). At higher positions, area per leaf again declined. Each successive leaf above leaf 3 averaged approximately 80 cm 2 larger than the preceding leaf, providing there was no floral initiation. Species did differ in the average rate of increase with leaf position with B. napus being fastest (100 cm 2 per leaf position) and B. carinata slowest (60 cm 2 per leaf, Fig. 6a). Time of planting had little effect on the shapes of the leaf area profiles, all profiles following the average trends shown in Fig. 6a. Planting time did have an effect however, on the scaling of the profiles. This is demonstrated in Fig. 6b which shows the leaf area profiles for the first, third and fifth plantings of B. napus. The largest leaves were produced from the first planting and the smallest from the last. The rationale for the pattern is shown in Fig. 7 where the area of the largest leaf at each planting date is plotted separately for each species, against the position of the leaf that was emerging at the time of floral initiation. The first point to be made from Fig. 7 is that the area of the largest leaf changed substantially with planting date for all species. Second, the position of the leaf that was emerging at floral initiation also changed substantially 35
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Days from sowing to floral initiation Fig. 5. Relationships between the duration of the period between sowing and floral initiation and final leaf number averaged for planting date in the four Brassica species.
R. Nanda et al. / Field Crops Research 42 (1995) 125-134 20
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at planting dates 1, 3 and 5 ( b ) .
(e.g. from 15 to 29 in B. carinata). And third, that the two were correlated though the relationships differed between species. Thus, there was strong evidence that if floral initiation was delayed in plant ontogeny to higher leaf positions, the leaf area profile developed further, and total plant leaf area increased. Consequently, not only was phenology having a marked effect on leaf number, but also on area per leaf and, by combination, leaf area per plant. As in sunflower (Rawson and Dunstone, 1986) the period for which each leaf expanded did not change with leaf position above leaf 3, and so it was the rate of expansion that determined the final size of each leaf. Thus, on average across species, each leaf expanded for 24.5 + 0 . 4 9 days or 360--410°Cd> 0°C (cf. sunflower varieties from 380-500°Cd, Rawson and Dunstone, 1986). However, durations of expansion for 1400
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leaves were significantly different between Brassica species, ranging from 2 1 . 5 + 0 . 4 2 days (B. campestris), to 24.1 -t- 0.52 days (B. juncea and B. carinata), to 26.8 +0.74 days (B. napus).
4. Discussion The aim of this study was to uncover some of the main differences between the Brassica species in terms of their determinants of leaf area production and where possible to reveal the sources of the differences. At first glance the species are very different with final leaf numbers ranging threefold, the largest leaves varying twofold in area, and new leaves appearing at rates differing by more than 30%. Also patterns at the sowing dates appear different with more and bigger leaves at earlier sewings, and the first leaf emerging earlier. Fortunately, we have tools and knowledge at our disposal to help us to understand the data. First, we have the concept of thermal time (Nuttonson, 1948; Monteith, 1984) which has been used so effectively to examine the effects of the environment on phenological development by negating the major effects of temperature (and see Rawson, 1993b for some draw backs of the concept). Second, we have the knowledge that phenological development feeds back strongly on the production of leaf number and leaf area (Rawson and Hindmarsh, 1982; Rawson, 1990), so environmental effects on phenology can also indirectly change patterns of accumulation of leaf area. And third, we know that the area of a leaf is part of a progression of areas established in preceding leaves and the progression itself is determined by the size of the leaf primordia
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R. Nanda et al. / Field Crops Research 42 (1995) 125-134
(see Rawson and Dunstone, 1986 and associated papers on sunflower). Taking the third point first to examine why areas of specific leaves were different amongst species, we would expect that the species with large early leaves would also have large later leaves. This idea holds well in that linear regressions between the area of leaf 2 and leaf 5 using data of B. campestris, B. juncea, and B. napus had r2 values of 0.999 (i.e.B. napus had the biggest second leaf and also the largest fifth leaf). However, while relationships with leaf 2 continued to hold for the areas of leaves 7 and 10, the r 2 values declined from 0.958 (leaf 7) to 0.678 (leaf 10), and declined even further to non-significance for higher leaves. We can explain the weakening of the relationship across species by their increasingly differing phenological states. Thus, by the time leaf 10 unfolded, floral initiation was already apparent in B. carnpestris and B. juncea, though not in B. napus, and so the areas of the latest leaves, and more specifically the sizes of their primordia, had been reduced by feed back from the developing floral organs (see Rawson and Turner, 1982 for an expansion of these arguments). B. carinata fits none of the above patterns which were otherwise common amongst the species. It had a large second leaf, but built up the areas of successive leaves relatively slowly. It also reached a peak area per leaf well before floral initiation occurred. These two facts suggest that the constraints to leaf primordia production and expansion at the growing apex might be different to those in the other species (see Williams, 1974 for likely constraints). Common relationships amongst species also explain differences in the final numbers of leaves achieved. Thus, the main plant variable associated positively with final leaf number was the duration of the period between sowing and floral initiation and one general relationship (Fig. 5) applied to all species. Clearly there was some flexibility within that general pattern because the first 15 leaves appeared at somewhat different rates amongst species with B. napus being slowest (and incidentally also having the longest duration of expansion and achieving the largest individual leaf areas), and B. campestris fastest ( B. campestris also had the shortest duration of leaf expansion). So rate and duration did interact to produce a final leaf number and consequently, any assessment of final leaf number must consider both of these variables.
Returning now to the tool of thermal time used so widely in studies of plant development, in the present data it convincingly explained a major difference between sowing dates in the time of emergence of the first leaf. Germination, emergence and early growth of the plants were therefore very much dependent on temperature. Also, for this phase, we could confirm the use of a base temperature of 5°C as calculated by Morrison et al. (1989) for summer rape grown in western Canada. However, once we had removed that variation in early growth due to temperature, leaf appearance rates expressed as leaves per calendar time after leaf 1, were similar amongst sowing dates. Surprisingly, expressing leaf appearance rates as leaves per thermal time (or as phyllochrons) did not reduce variation in this parameter between sowing dates (Fig. 2).Inother words, in the environment of the study, leaf number at any time after the appearance of leaf one, would be equally well predicted by using a relationship based on leaves per day as on one using leaves per degree day. We should add here that average phyllochron for the study was not at variance with that of 46°Cd calculated for summer rape by Morrison and McVetty ( 1991 ). This finding that calendar time is as good a predictor of leaf appearance rate as thermal time indicates that other subsidiary environmental variables associated with season are equally as important in driving leaf appearance rates as is temperature. One such minor variable, radiation, changed leaf appearance rates by 27% in field crops of sunflower (Rawson and Hindmarsh, 1983). The parallel of this in the Brassica studies is that some of the increase in rates of leaf appearance of upper leaves in late plantings could have been associated with increases in radiation, associated, in turn, with longer days. However, more important than any direct effects of these subsidiary environmental factors on leaf appearance rates is likely to be the indirect effect of changed phenology. In these studies, increases of up to 50% in rate of appearance of leaves occurred after floral initiation (Fig. 2). This was apparent even when rate was measured in thermal time (Fig. 2), and so ostensibly the effects of increased temperature with advancement of the season were removed. Phenological development is driven by temperature, both mean and vernalising temperatures, and by photoperiod (Hodgson, 1978a, b), and in some circumstances by radiation (Rawson, 1993a). These environmental factors can covary. Thus, short photoperiod
R. Nanda et al. / FieM Crops Research 42 (1995) 125-134
is associated with reduced peak radiation, reduced daily radiation, lower mean temperature, and lower minimum temperature. Of these, low minimum temperature would advance phenology in thermal time (Hodgson, 1978a), while both short photoperiod and low radiation could have the reverse effect of slowing phenological development in the Brassica species. The point that is being made here is that if environment is affecting the rate of leaf production and growth in area both through direct effects on the leaves and indirectly through phenological processes, and if the effects are interacting, calendar time can be a better integrator of the main effects than thermal time. Before thermal time can become the more useful measure, more knowledge is required of the direct and indirect responses of each species to vernalisation and mean temperature, and to photoperiod. One aim of this study was to determine if there are common factors across these superficially very different Brassica species which are controlling the production of crop leaf area. It seems that phenological development has a universal feed back on leaf area both through the final number of leaves and the areas of individual leaves. If we can understand the main effects of the environment on phenological development in each of the species, specifically the effects of vernalising temperatures, temperature per se, and photoperiod, and also gauge the importance of the interactions between these factors, we will have progressed towards understanding the differences in leaf area production between sites, times and species. The data here suggest, however, that there are other factors, aside from phenology, which affect the production of leaf area amongst species. It is suggested that events on the apical dome during primordia production are likely to account for many of these differences.
References Angus, J.F., MacKenzie, D.H., Morton, R. and Schafer, C.A., 1981. Phasic development in field crops. II. Thermal and photoperiodic responses of spring wheat. Field Crops Res., 4: 269-283. Campbell, C.D. and Kondra, Z.P., 1977. Growth pattern analysis of three rapeseed cultivars. Can. J. Plant Sci., 57: 707-712. Clarke, J.M. and Simpson, G.M., 1978. Growth analysis of Brassica napus cv. Tower. Can. J. Plant Sci., 58: 587-595.
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Coelho, D.T. and Dale, R.F., 1980. An energy-crop growth variable and temperature function for predicting corn growth and development: planting to silking. Agron. J., 72:503-510. Gallagher, J.N., 1979. Field studies of cereals leaf growth. I. Initiation and expansion in relation to temperature and ontogeny. J. Exp. Bot., 30: 625-636. Gotch, T., 1977. Varietal differences in photoperiodic and thermal responses of wheat. Jpn. J. Breed., 27:57-69 (in Japanese). Hodgson, A.S., 1978a. Rapeseed adaptation in Northern New South Wales. I. Phenological responses to vernalization, temperature and photoperiod by annual and biennial cultivars of Brassica campestris L., Brassica napus L. and wheat cv. Timgalen. Aust. J. Agric. Res., 29: 693-710. Hodgson, A.S., 1978b. Rapeseed adaptation in Northern New South Wales. 11. Predicting plant development of Brassica campestris L. and Brassica napus L. and its implications for planting time, designed to avoid water deficit and frost. Aust. J. Agric. Res., 29:711-726. Hofstra, G.J., Hesketh, J.D. and Myhre, D.L., 1977. A plastochron model for soybean leaf and stem growth. Can. J. Plant Sci., 57: 167-175. Kasa, G.R. and Kondra, Z.P., 1986. Growth analysis of springtype oilseed rape. Field Crops Res., 14: 361-370. Moncur, M.W., 1981. Floral Initiation in Field Crops: An Atlas of Scanning Electron Micrographs. CSIRO, Melbourne. Monteith, J.L., 1984. Consistency and convenience in the choice of units for agricultural science. Exp. Agric., 20: 125-137. Morrison, M.J. and McVetty, P.B.E., 1991. Leaf appearance rates in summer rape. Can. J. Plant Sci., 71: 405-412. Morrison, M.J., McVetty, P.B.E. and Shaykewich, C.F., 1989. The determination and verification of a baseline temperature for the growth of westar summer rape. Can. J. Plant Sci., 69: 455-464. Nuttonson, M.Y., 1948. Some preliminary observations of phenological data as a tool in the study of photoperiod and thermal requirement of various plant material. In: A.E. Murneck and R.O. Whyte (Editors), Vernalization and Photoperiodism: A Symposium. Chronica Botanica Co., Waltham, MA, pp. 129-143. Rawson, H.M., 1990. Can productivity in sunflower be increased by changed plant development? In: S.K. Sinha, P.V. Sane, S.C. Bhargava and P.K. Agrawal (Editors), Proceedings of the International Congress of Plant Physiology, New Delhi, India, pp. 361-372. Rawson, H.M., 1993a. Radiation effects on rate of development in wheat grown under different photoperiods and high and low temperatures. Aust. J. Plant Physiol., 20: 719-727. Rawson, H.M., 1993b. Prediction of heading time in wheat grown under high temperatures: effects of temperature, vernalisation and photoperiod. Indian J. Plant Physiol., 36: 243-249. Rawson, H.M. and Dunstone, R.L., 1986. Simple relationships describing the responses of leaf growth to temperature and radiation in sunflower. Aust. J. Plant Physiol., 13:321-327. Rawson, H.M. and Hindmarsh, J.H., 1982! Effects of temperature on leaf expansion in sunflower. Aust. J. Plant Physiol., 9: 209219. Rawson, H.M. and Hindmarsh, J.H., 1983. Light, leaf expansion and seed yield in sunflower. Aust. J. Plant Physiol., 10: 25-30.
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Rawson, H.M. and Turner, N.C., 1982. Recovery from water stress in five sunflower (Helianthus annuus L.) cultivars. II. The development of leaf area. Aust. J. Plant Physiol., 9: 449--460. Rawson~ H.M. and Turner, N.C., 1983. Irrigation timing and relationships between leaf area and yield in sunflower. Irrigation Sci., 4: 167-175. Robertson, G.W. and Russel, D.A., 1968. Astrometeorological estimator for estimating time when sun is at any elevation in the morning and afternoon and hourly and daily values of solar energy, Qo. Agricultural Meterology, Technical Bulletin, Canada Department of Agriculture, 14:22. Sinclair, T.R., 1984. Leaf area development in field grown soybean. Agron. J., 76: 141-146. Slafer, G.A. and Rawson, H.M., 1994. Sensitivity of wheat phasic development to major environmental factors: a re-examination of some assumptions made by physiologists and modellers. Aust. J. Plant Physiol., 21: 393-426.
Slafer, G.A. and Rawson, H.M., 1995. Intrinsic earliness and basic development rate assessed for their response to temperature in wheat genotypes. Euphytica (in press ). Slafer, G.A., HaUoran, G.M. and Connor, D.J., 1994a. Development rate in wheat as affected by duration and rate of change of photoperiod. Ann. Bot., 73:671-677. Slafer, G.A., Connor, D.J. and Halloran, G.M., 1994b. Rate of leaf appearance and final numbers of leaves in wheat: Effects of duration and rate of cchange of photoperiod. Ann. Bot., 74: 427436. Thurling, N., 1974. Morphophysiological determinants of yield in rapeseed ( Brassica campestris and Brassica napus ). I. Growth and morphological characters. Aust. J. Agric. Res., 25:697-710. Watson, D.J., 1956. Leaf growth in relation to crop yield. In F.L. Milthorpe (Editor), Growth of Leaves. Butterworths, London, pp. 178-191. Williams, R.F., 1974. The Shoot Apex and Leaf Growth. Cambridge University Press, London.
ELSEVIER
Field Crops Research 42 (1995) 125-134
Field Crops Research
Effect of sowing date on rates of leaf appearance, final leaf numbers and areas in Brassica campestris, B. juncea, B. napus and B. carinata R. Nanda a, S.C. Bhargava a, H.M. Rawson b,. ~Division of Plant Physiology, Indian Agricultural Research Institute, New Delhi-llO 012, India b Division of Plant Industry, CSIRO, GPO Box 1600, Canberra, A.C.T. 2601, Australia
Received 26 July 1994; accepted 13 May 1995
Abstract B. campestris (cv. Pusa Kalyani), B.juncea (cv. Varuna), B. napus (cv. BO 706) and B. carinata (cv. Tall-1 ) were studied in the field at five dates of sowing during one cropping season. Photoperiod at the successive sowing dates declined from 11.310.2 h and mean temperature from 24 to 15°C. Planting date had a big effect on the duration to the appearance of the first leaf with the range being from 10.8 (sowing 1) to 22 days after sowing (sowing 5), equivalent to a delay of 1.35 days for each I°C reduction in mean temperature. Base temperatures for this phase were approximately 5°C for all species. Planting date had no significant effect on the rate of appearance of subsequent leaves which ranged between 2.68 (date 1) and 2.84 days per leaf (date 3) and averaged equivalent to 0.37 + 0.003 leaves per day. However, rates of leaf appearance differed over a 35% range amongst species, with new leaves appearing every 2.33 _ 0.07 days (B. campestris), 2.71 + 0.12 (B. juncea), 2.90_+ 0.09 (B. carinata), and 3.18 + 0.08 days (B. napus). Upper leaves emerged between 33 and 48% faster than lower leaves depending on species, and this was most apparent at the final two sowings, and particularly in B. napus. Final leaf number declined with later sowing at a rate ranging between 0.186 (B. campestris) and 0.112 leaves per day (B. juncea). Absolute numbers differed amongst species from 35 (B. carinata, sowing 1) to 12 (B. campestris, sowing 5), but were positively correlated with days from sowing to floral initiation. Area per leaf increased with leaf position reaching a peak in the leaf that was emerging at approximately the time of floral initiation with B. napus leaves on average increasing fastest ( 100 cm2 per leaf position) and B. carinata slowest (60 cm2 per leaf). Planting date affected areas of individual leaves largely through changing the timing of floral initiation and by consequence the degree of advancement of the leaf area profiles. It is concluded that although some of the leaf number and area characteristics are under the control ofphenological development, there is considerable variation amongst species aside from this. Keywords: Brassica; Date of sowing;Leaf area; Leaf number;Managementpractices; Phenology
1. Introduction Leaf area per unit ground area determines the percentage of solar radiation intercepted by a crop and * Correspondingauthor. 0378-4290/95/$09.50 © 1995 ElsevierScienceB.V. All rights reserved S S D I 0 3 7 8 - 4 2 9 0 ( 9 5 ) 00026-7
therefore has a predominant influence on crop growth (Watson, 1956; Sinclair, 1984). The rate of establishment of leaf area after sowing is particularly important to subsequent crop growth (Gallagher, 1979). Thurling (1974) and Clarke and Simpson (1978) con-
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R. Nanda et al. / Field Crops Research 42 (1995) 125-134
cluded that in summer rape, seed yield and maximum leaf area index are positively correlated and similar conclusions have been reached for irrigated sunflower (Rawson and Turner, 1983). Though these correlative observations have been made, there are few comparative studies of several Brassica species in the field to establish whether there are differences amongst species in their rates of leaf area establishment, their final leaf areas, and particularly the means by which they achieve their final leaf numbers and areas. Furthermore, there are few field studies which have attempted to examine how environmental factors may change the parameters of leaf area production. To quantify leaf development in soybean (Glycine max. L.), Hofstra et al. (1977) described it in terms of leaf appearance rate, leaf area expansion rate, maximum leaf area and leaf area duration. A similar analytical approach in Brassica species would demonstrate whether there are differences in these parameters among species and even whether there might be scope for inter-species hybridisation to improve the rate of crop leaf area development. It is likely that environmental variables will change these parameters as occurs in sunflower (e.g. Rawson and Dunstone, 1986), and possibly even change them differentially amongst the species. For example, one of those environmental variables, temperature, affects many plant processes and especially plant development (Coelho and Dale, 1980; Slafer and Rawson, 1994), and has been shown in wheat to affect cultivars differentially in phenological development and leaf emergence (Slafer and Rawson, 1995). Consequently, in any study of development it
is important to establish whether the parameters of interest are changed by the environment, and if so, to what degree. The present study describes the changes that occur in several parameters of leaf area production when planting date is changed in the field and compares four Brassica species for their responses.
2. Material and methods
Four species of Brassica, B. campestris cv. Pusa Kalyani; B. juncea cv. Varuna, B. napus cv. BO-706 and B. carinata cv. Tall-1 were planted at intervals during the cropping season of 1991-92. Sowings were on 19 and 29 October, 8 and 28 November, and 9 December, in 5 × 4 m plots with 45 × 20 cm spacing thus giving 12 plants m -2. N, P and K at 40:40:40 kg h a - ] was applied before sowing. After germination, six plants in 1 m row length in each treatment were selected for observations. All leaves on these plants were tagged and numbered in sequence from the base to the top of the plant when they were about 1 cm long. Leaf length and breadth were measured at the widest point of the blade every second or third day until maximum length was reached and final area was estimated for each leaf from the product of maximum length and breadth. Detailed observations were taken on 15 leaves in early cultivars and 20 leaves in late-maturing cultivars. Rates and durations of leaf area expansion was estimated by fitting second-order polynominal equations to the data of area by time in days for each leaf.
,0
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Fig. 1. Environmental variables in days after the first planting. Screen maximum and minimum temperatures (a) and (b) photoperiod (hours) and rate of change of daylength in minutes per day plus 10 minutes (i.e. the line of no change is at 10 minutes). On these figures the five plantings were on days 1, 11,21, 41, and 52.
R. Nanda et al. / Field Crops Research 42 (1995) 125-134
Records of daily maximum and minimum temperature (Fig. la) were obtained from the Indian Agricultural Research Institute Meteorological Station located less than 100 m away from the experimental site. Degree days with units of °Cd were calculated by accumulating the mean of these maximum and minimum temperatures above a base temperature of 0°C. The °Cd sums were accumulated independently for each leaf or each growth stage. Assuming a critical light intensity of 15 lux for photoperiodic response of wheat (Gotch, 1977), it was determined graphically that this requirement would be met when the sun is at an elevation of more than -3053 '. Daily values of photoperiodic day-length were therefore taken as the duration of the day when angle exceeded this value following Robertson and Russel (1968). The hour values of photoperiod calculated, and the rates in minutes at which photoperiod changed each day are shown on Fig. lb. On the figure, sowing dates were equivalent to days 1, 11, 21, 41, and 52 for the five respective plantings. As can be seen, photoperiod at planting reduced over a relatively narrow range from 11.3 to 10.2 h amongst sowing dates and photoperiods only started to increase some 10 days after the last planting. Mean temperatures at sowing changed from 24 to 15°C.
3. Results
3.1. Leaf emergence Although temperature and photoperiod were changing throughout the study, leaves appeared approximately linearly with time after sowing in all species (Fig. 2a, d, g, j ). Linear regressions fitted between leaf position and time, considering each sowing date and species separately, all had coefficients of determination which were better than r 2 = 0.95. Averaging across species, a new leaf appeared every 2.78 ___0.03 days, with a small range amongst planting dates of from 2.68 (planting 1) to 2.84 days per leaf (planting 3). The overall mean value is equivalent to 0.37 + 0.003 leaves per day (cf. values of 0.35-0.40 leaves/day for summer rape according to Campbell and Kondra (1977)). However, average rates of leaf appearance differed amongst species over a 35% range with new leaves appearing every 2.33+0.07 days (B. campestris),
127
2.71 ___0.12 (B.juncea), 2.90__+ 0.09 (B. carinata), and 3.18-t-0.08 days (B. napus). These results support those of Kasa and Kondra, 1986) who found that B. campestris had a higher leaf emergence rate than B. napus during all growth periods. The main difference between planting dates in the time taken between sowing and the appearance of any leaf was not the slopes or rates of leaf appearance, but the intercepts i.e. when the first leaf appeared after crops were sown. Thus, on average across species, and for the respective sowing dates, leaf 1 appeared on day 10.8+0.31 (sowing 1), 12.6+__1.00 (2), 13.6+__1.06 (3), 18.9+ 1.13 (4), and day 22.0+0.39 (5) after sowing. The day of appearance of leaf 1 was well correlated linearly and inversely with the temperatures between sowing and that day, with no apparent statistical difference in the effect of maximum, mean, or minimum temperatures. Thus, using the mean temperature, the appearance of leaf 1 was delayed by 1.35 days for each 1°C reduction in temperature. Using the same data to calculate the base temperature for time to leaf 1 (i.e. regressing 1/days between sowing and leaf 1 against mean temperature for that period, see Angus et al., 1981), the range was between 4.1 and 5.5°C, depending on which data points were included (cf. 5°C estimated by Morrison et al., 1989 for summer rape grown in western Canada). Base temperatures thus calculated for B. campestris, B. juncea, B. napus, and B. carinata respectively were 5.7, 6.6, 4.6, and 5.3°C. Clearly, there were no marked differences between species in this parameter. We have redrawn the curves of Fig. 2a, d, g, j (after removing from the x-axis the calculated number of days between sowing and leaf 1 emergence), as Fig. 2b, e, h, k, respectively, to see whether most of the variation between sowings in time of leaf appearance is due to differences in time of appearance of the first leaf. Visually this appears to be the case. It also seems to be the case statistically, since if we then fit linear regressions through the combined data sets for each species, we see that the variance ratios ( F values) have increased from 384 to 1275 (Fig. 2a vs 2b, B. campestris), 538 to 1312 (Fig. 2d vs 2e, B.juncea), 87 to 1826 (Fig. 2g vs 2h, B. napus) and from 400 to 2242 (Fig. 2j vs 2k, B. carinata ) . If temperature is the main factor affecting the time between sowing and appearance of leaf 1, as seems to be supported from the above analysis, we might expect
R. Nanda et al. / Field Crops Research 42 (1995) 125-134
128
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Fig. 2. T i m e o f e m e r g e n c e for e a c h leaf o f the four Brassica species, w h e r e time is m e a s u r e d in days after sowing (a, d, g, j ), in days after leaf 1 e m e r g e d (b, e, h, k ) , or in thermal time after s o w i n g (c, f, i, 1). The five curves on each figure are for e a c h o f the five planting dates: 19, 29 October, 8, 28 N o v e m b e r a n d 9 December.
129
R. Nanda et al. / Field Crops Research 42 (1995) 125-134
Planting date 2
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Fig. 3. Effect of planting date on rate of change in phyllochron ( + 2 X se) between leaves 1 and 15 (a). Also shown are rate of change of photoperiod (open squares, a) and minimum temperatures (b) for these plantings using mean daily data between sowing and the appearance of leaf 8. Planting dates were 19, 29 October, 8, 28 November and 9 December.
that differences in temperature might be causing any spread of response in the rates of appearance of subsequent leaves. The analysis in Fig. 2c, f, i, and 1, where thermal time (°Cd > 0°C) is substituted for days, does not appear to support that proposition, as F values for linear regressions through the data are smaller than those using only calendar time as the x-axis (respective F values for species were 700, 1183, 1141, and 1925). We have used 0°C as the base temperature in this figure, rather than the 5°C suggested by Morrison et al. (1989), but that will have no effect on the relationships shown. What we have assumed thus far, to keep the analysis simple, is that upper and lower leaves appear at much the same rate. In fact, upper leaves often appeared faster (and so had shorter phyllochrons) than lower leaves and this was particularly true for B. campestris and B. napus for the later sowings. This difference is demonstrated by comparing the linear regressions between leaf position and thermal time averaged across sowings for leaves 1-6 and for 7-15. Thus, for B. campestris, B. juncea, B. napus, and B. carinata, mean phyllochrons (°Cd> 0°C/leaf) for leaves 1-6 were 59.9, 64.9, 82.6 and 63.7°Cd respectively, and for leaves 7-15 were 31.3, 40.7, 45.2 and 42.9°Cd. This shows that there was a reduction in phyllochron associated with higher leaf position in all species. In relative terms the reduction was 48, 37, 45, and 33% for the respective species. Further examination of Fig. 2 indicates that it is the later sowings that show the greatest reduction in phyllochron with sowing date. If we now test this visual assessment by regression, we find that phyllochron is
decreasing on average across species from leaves 1-15 for the five sowing dates by 1.92 i- 0.60, 2.63 4- 0.64, 2.02+0.86, 4.91 +0.49, and 3.28_0.38°Cd per leaf respectively. All species had their greatest reduction with leaf position at sowing 4 with the response by B. napus being greatest and that in B. carinata least. The average pattern is shown in Fig. 3a. Also shown in Fig. 3 is the rate of change of photoperiod at the time of emergence of leaf 7 (see Slafer et al., 1994a, b for a discussion of the importance to phenological development of rate of change of photoperiod) and the mean minimum temperature between sowing and emergence of leaf 7 for sowings 1-5. Minimum temperature may have some impact on accelerating phenology through its effect on satisfying a vernalisation response (see Hodgson, 1978a for responses of B. campestris and B. napus to vernalisation). Clearly there are associations between rate of change of phyllochron and the weather parameters shown in Fig. 3. For example, it would be possible to argue that the considerably more rapid development of upper leaves at sowings 4 and 5 was associated with photoperiods starting to lengthen at that time, and with temperatures reaching values which would accelerate the vernalisation process. Whether the associations are causal cannot be assessed without controlled environment experimentation. However, from the above data on change in phyllochron, we might guess that B. napus is one of the more sensitive species to these parameters. 3.2. Final leaf number We have analysed only the first 15 leaves on each species for rate of appearance, but there were many
130
R. Nanda et al. / Field Crops Research 42 (1995) 125-134 40
3.3. Leaf area
35
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--=-juncea napus ; --M-carinata 0
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2 3 4 Planting date
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Fig. 4. Final leaf numbers for the four Brassica species from each of the five planting dates (19, 29 October, 8, 28 November and 9 December).
more leaves produced particularly in the later lines B. napus and B. carinata. These were all counted to show that final leaf number also changed with sowing date, with a universal reduction in number with later planting under lengthening photoperiods and lower temperatures (Fig. 4). The rate of reduction with sowing date was the same in B. napus and B. carinata (0.167 and 0.168 leaves per day for days after 19 October, r 2 = 0.93 and 0.97) with a 33% lower slope in B. juncea ( - 0 . 1 1 2 leaves day -~, P = 0 . 9 8 4 ) and a slightly greater slope in B. campestris ( - 0.186 leaves day- ~, P = 0 . 9 9 1 ) . However, the much greater differences between the species than the rates of change with sowing date, were the calculated intercepts at the first sowing of 20.6, 18.2, 26 and 35.2 leaves for B. campestris, B. juncea, B. napus, and B. carinata respectively. This indicates that the absolute responses to the changing environment (cold and photoperiod) in terms of leaf number differed only marginally between species, but that the environmental parameters determining basal leaf number must differ substantially between species. The environmental parameters determining final leaf number are most likely to be those which step the plant through from primarily vegetative, to primarily floral development i.e. that determine phenological development. This notion is given support in Fig. 5 which shows the significant linear correlation between the final number of leaves (y) for each species and the number of days each species takes from sowing to floral initiation (x). The species which flowered early also had few leaves.
All four species followed the pattern of leaf area vs leaf position shown by dicots with an apical meristem which expands laterally with age (cf. Moncur, 1981, and see the similarities with sunflower in Rawson and Dunstone, 1986). Thus, in general, area per leaf increased with successive leaves (Fig. 6a), reaching a peak in three of the species in the leaf that was emerging at approximately the time of floral initiation ( see later). At higher positions, area per leaf again declined. Each successive leaf above leaf 3 averaged approximately 80 cm 2 larger than the preceding leaf, providing there was no floral initiation. Species did differ in the average rate of increase with leaf position with B. napus being fastest (100 cm 2 per leaf position) and B. carinata slowest (60 cm 2 per leaf, Fig. 6a). Time of planting had little effect on the shapes of the leaf area profiles, all profiles following the average trends shown in Fig. 6a. Planting time did have an effect however, on the scaling of the profiles. This is demonstrated in Fig. 6b which shows the leaf area profiles for the first, third and fifth plantings of B. napus. The largest leaves were produced from the first planting and the smallest from the last. The rationale for the pattern is shown in Fig. 7 where the area of the largest leaf at each planting date is plotted separately for each species, against the position of the leaf that was emerging at the time of floral initiation. The first point to be made from Fig. 7 is that the area of the largest leaf changed substantially with planting date for all species. Second, the position of the leaf that was emerging at floral initiation also changed substantially 35
=. 30
y = 0.4966x+ 0.0926 / R2= 0.g9
= 20
.s u. 15
10 20
30
40
50
60
70
Days from sowing to floral initiation Fig. 5. Relationships between the duration of the period between sowing and floral initiation and final leaf number averaged for planting date in the four Brassica species.
R. Nanda et al. / Field Crops Research 42 (1995) 125-134 20
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Area of leaf ( c m =)
F i g . 6. Profiles of area per leaf against leaf position from the base of the plant (leaf 1 ) for each of the four Brassica species ( a ) and for B. napus
at planting dates 1, 3 and 5 ( b ) .
(e.g. from 15 to 29 in B. carinata). And third, that the two were correlated though the relationships differed between species. Thus, there was strong evidence that if floral initiation was delayed in plant ontogeny to higher leaf positions, the leaf area profile developed further, and total plant leaf area increased. Consequently, not only was phenology having a marked effect on leaf number, but also on area per leaf and, by combination, leaf area per plant. As in sunflower (Rawson and Dunstone, 1986) the period for which each leaf expanded did not change with leaf position above leaf 3, and so it was the rate of expansion that determined the final size of each leaf. Thus, on average across species, each leaf expanded for 24.5 + 0 . 4 9 days or 360--410°Cd> 0°C (cf. sunflower varieties from 380-500°Cd, Rawson and Dunstone, 1986). However, durations of expansion for 1400
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Leaf emerging at Floral Initiation F i g . 7. Area of the largest leaf produced by the plant from each of
the five planting dates, against the position of the leaf that was emerging at the time of floral initiation, plotted separately for each species. No regression is shown for B.juncea.
leaves were significantly different between Brassica species, ranging from 2 1 . 5 + 0 . 4 2 days (B. campestris), to 24.1 -t- 0.52 days (B. juncea and B. carinata), to 26.8 +0.74 days (B. napus).
4. Discussion The aim of this study was to uncover some of the main differences between the Brassica species in terms of their determinants of leaf area production and where possible to reveal the sources of the differences. At first glance the species are very different with final leaf numbers ranging threefold, the largest leaves varying twofold in area, and new leaves appearing at rates differing by more than 30%. Also patterns at the sowing dates appear different with more and bigger leaves at earlier sewings, and the first leaf emerging earlier. Fortunately, we have tools and knowledge at our disposal to help us to understand the data. First, we have the concept of thermal time (Nuttonson, 1948; Monteith, 1984) which has been used so effectively to examine the effects of the environment on phenological development by negating the major effects of temperature (and see Rawson, 1993b for some draw backs of the concept). Second, we have the knowledge that phenological development feeds back strongly on the production of leaf number and leaf area (Rawson and Hindmarsh, 1982; Rawson, 1990), so environmental effects on phenology can also indirectly change patterns of accumulation of leaf area. And third, we know that the area of a leaf is part of a progression of areas established in preceding leaves and the progression itself is determined by the size of the leaf primordia
132
R. Nanda et al. / Field Crops Research 42 (1995) 125-134
(see Rawson and Dunstone, 1986 and associated papers on sunflower). Taking the third point first to examine why areas of specific leaves were different amongst species, we would expect that the species with large early leaves would also have large later leaves. This idea holds well in that linear regressions between the area of leaf 2 and leaf 5 using data of B. campestris, B. juncea, and B. napus had r2 values of 0.999 (i.e.B. napus had the biggest second leaf and also the largest fifth leaf). However, while relationships with leaf 2 continued to hold for the areas of leaves 7 and 10, the r 2 values declined from 0.958 (leaf 7) to 0.678 (leaf 10), and declined even further to non-significance for higher leaves. We can explain the weakening of the relationship across species by their increasingly differing phenological states. Thus, by the time leaf 10 unfolded, floral initiation was already apparent in B. carnpestris and B. juncea, though not in B. napus, and so the areas of the latest leaves, and more specifically the sizes of their primordia, had been reduced by feed back from the developing floral organs (see Rawson and Turner, 1982 for an expansion of these arguments). B. carinata fits none of the above patterns which were otherwise common amongst the species. It had a large second leaf, but built up the areas of successive leaves relatively slowly. It also reached a peak area per leaf well before floral initiation occurred. These two facts suggest that the constraints to leaf primordia production and expansion at the growing apex might be different to those in the other species (see Williams, 1974 for likely constraints). Common relationships amongst species also explain differences in the final numbers of leaves achieved. Thus, the main plant variable associated positively with final leaf number was the duration of the period between sowing and floral initiation and one general relationship (Fig. 5) applied to all species. Clearly there was some flexibility within that general pattern because the first 15 leaves appeared at somewhat different rates amongst species with B. napus being slowest (and incidentally also having the longest duration of expansion and achieving the largest individual leaf areas), and B. campestris fastest ( B. campestris also had the shortest duration of leaf expansion). So rate and duration did interact to produce a final leaf number and consequently, any assessment of final leaf number must consider both of these variables.
Returning now to the tool of thermal time used so widely in studies of plant development, in the present data it convincingly explained a major difference between sowing dates in the time of emergence of the first leaf. Germination, emergence and early growth of the plants were therefore very much dependent on temperature. Also, for this phase, we could confirm the use of a base temperature of 5°C as calculated by Morrison et al. (1989) for summer rape grown in western Canada. However, once we had removed that variation in early growth due to temperature, leaf appearance rates expressed as leaves per calendar time after leaf 1, were similar amongst sowing dates. Surprisingly, expressing leaf appearance rates as leaves per thermal time (or as phyllochrons) did not reduce variation in this parameter between sowing dates (Fig. 2).Inother words, in the environment of the study, leaf number at any time after the appearance of leaf one, would be equally well predicted by using a relationship based on leaves per day as on one using leaves per degree day. We should add here that average phyllochron for the study was not at variance with that of 46°Cd calculated for summer rape by Morrison and McVetty ( 1991 ). This finding that calendar time is as good a predictor of leaf appearance rate as thermal time indicates that other subsidiary environmental variables associated with season are equally as important in driving leaf appearance rates as is temperature. One such minor variable, radiation, changed leaf appearance rates by 27% in field crops of sunflower (Rawson and Hindmarsh, 1983). The parallel of this in the Brassica studies is that some of the increase in rates of leaf appearance of upper leaves in late plantings could have been associated with increases in radiation, associated, in turn, with longer days. However, more important than any direct effects of these subsidiary environmental factors on leaf appearance rates is likely to be the indirect effect of changed phenology. In these studies, increases of up to 50% in rate of appearance of leaves occurred after floral initiation (Fig. 2). This was apparent even when rate was measured in thermal time (Fig. 2), and so ostensibly the effects of increased temperature with advancement of the season were removed. Phenological development is driven by temperature, both mean and vernalising temperatures, and by photoperiod (Hodgson, 1978a, b), and in some circumstances by radiation (Rawson, 1993a). These environmental factors can covary. Thus, short photoperiod
R. Nanda et al. / FieM Crops Research 42 (1995) 125-134
is associated with reduced peak radiation, reduced daily radiation, lower mean temperature, and lower minimum temperature. Of these, low minimum temperature would advance phenology in thermal time (Hodgson, 1978a), while both short photoperiod and low radiation could have the reverse effect of slowing phenological development in the Brassica species. The point that is being made here is that if environment is affecting the rate of leaf production and growth in area both through direct effects on the leaves and indirectly through phenological processes, and if the effects are interacting, calendar time can be a better integrator of the main effects than thermal time. Before thermal time can become the more useful measure, more knowledge is required of the direct and indirect responses of each species to vernalisation and mean temperature, and to photoperiod. One aim of this study was to determine if there are common factors across these superficially very different Brassica species which are controlling the production of crop leaf area. It seems that phenological development has a universal feed back on leaf area both through the final number of leaves and the areas of individual leaves. If we can understand the main effects of the environment on phenological development in each of the species, specifically the effects of vernalising temperatures, temperature per se, and photoperiod, and also gauge the importance of the interactions between these factors, we will have progressed towards understanding the differences in leaf area production between sites, times and species. The data here suggest, however, that there are other factors, aside from phenology, which affect the production of leaf area amongst species. It is suggested that events on the apical dome during primordia production are likely to account for many of these differences.
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