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Leaf demography in willow short-rotation coppice
Vol. 5, No. 5, PP. 325-336,1993 Printed in Great Britain. All rights reserved
0961-9534/93 56.00+O.OO
Biomass and Bioenergy
LEAF DEMOGRAPHY
0 1993Pergamon Press Ltd
IN WILLOW SHORT-ROTATION COPPICE
JOHNR. PORTER, RODNEY I. PARFITTand GILLIANM. ARNOLD Department of Agricultural Sciences, University of Bristol, AFRC Institute of Arable Crops Research, Long Ashton Research Station, Bristol, BS18 9AF, U.K. (Received 28 May 1993; accepted
13 August 1993)
Abstract-The production, survivorship and death of cohorts of leaves within the canopies of three clones (Sulix burjatica “Korso”, S. viminnlis “Mullatin” and S. x dnsyclados) of willow grown as short-rotation coppice were studied in a field experiment. The initial rate of increase in leaf number was fastest for “Mullatin”, which also had the steepest rate of decline in net leaf number. Inter-clonal variability was not reduced by plotting changes in leaf number against thermal time, accumulated above 0°C. Mean number of leaves was highest for “Mullatin” and least for “Korso”. Leaf production occurred in flushes and there were no significant clonal differences in the relative rate of leaf birth: differences in relative rate of leaf death (r,,) became apparent after day number 230 (1 Jan = 1); thereafter “Korso” had higher values of r, than the other clones. The time course of r, was summarked by a logistic curve and there was no evidence that the initial asymptote nor the maximal rate of change of r, differed between clones. Leaves of “Korso” had minimum and maximum longevities of about 25 days (or about 2SO”Cd in thermal time) and 65 days (about IOOO‘Cd),respectively; minimum leaf longevities for the other two clones were similar to that for “Korso” but their leaves lived for up to 100 days (about 14OOCd). Changes in the age-structure of the leaf populations with time were little influenced by differences in leaf demography between clones. A positive and significant correlation was found between the rate of production of leaves and temperature up to about 14°C. Thereafter, the correlation was either absent or negative. Results are interpreted in terms of the consequences of differences in canopy demography for coppice biomass production. Keywords-Canopy,
coppice, demography, leaves, willow.
1. INTRODUCTION
Previous work has shown that the dry matter productivity of many crops is related linearly to the quantity of photosynthetically active radiThis is also the case with ation they absorb. ‘*2*3 willows grown as a short-rotation crop and coppiced on a four-to-five year cycle.4 This relationship depends both on the efficiency of absorption of radiation per unit time and the duration of interception. Both processes are influenced by the architectural form of the leaf canopy of which an important determinant is the age-structure and population dynamics of shoots and leaves. Demographic studies of leaves and shoots have been made for Linum usitatissimum,’ Catapodium ~pp.,~ Ammophila arenaria,’ Lolium perenne,’ Carex arenaria 9 and Betula pendula and Pinus nigra.“,” Models of
canopy development based explicitly on the demographic behaviour of shoots and leaves have been developed for cereals.12
The photosynthetic activity of a canopy depends on the age-structure of its component leaves.13 MarshallI showed that the maximum rate of photosynthesis declined monotonically with age for the flag and penultimate leaves of wheat. Whereas stomata1 resistance did not increase greatly with leaf age, increases in mesophyll and carboxylation resistances to CO2 incorporation were found. Thus, in order to predict the dry matter production of a stand of willows or other perennial vegetation, knowledge of the demography of the leaf canopy is required. This study investigates the population dynamics of leaf populations of three clones of willow used in short-rotation coppice. The clones were chosen because they exhibit wide variation in their architectural form and because they are important varieties for biomass production. The study also links demographic parameters such as leaf birth and death rates to temperature. The consequences of differences 325
J. R. PORTERet
326
in the population dynamics of the leaf canopy for the age-structure, and by implication the efficiency of the canopy, are also assessed. 2. MATERIALS
AND METHODS
The production, survival and death of leaves on three clones of willow were censused from spring until autumn 1988 at Long Ashton Research Station, Bristol, U.K. (latitude 50.5”N). The clones chosen for study were Salix burjatica “Korso”, S. viminalis “Mullatin” and S. x dasyclados. At each census every fifth leaf, on selected shoots, in the group of leaves produced since the previous sampling was identified and tagged with differently coloured, non-toxic plastic tape. The complete group of leaves formed a cohort of leaves from which each fifth leaf was non-destructively and successively sampled throughout its lifetime. Measurements were taken from three replicate single clonal plots for each clone with 12 plants per replicate plot and two shoots were sampled per plant, chosen at random. Data were recorded for each sample leaf on a hand-held data logger (Epson HX-20) from which the results were passed to a mainframe computer for analysis. Leaf demographic measurement started on 18 April 1988 (day number 109) and continued until 21 November 1988 (day number 325). During this period there were 25 dates, at approximately weekly intervals, during which samples of leaves were assessed as being either living, dead but still attached to the shoot or dead and abscinded from the shoot. Although the sampling interval was approximately weekly, this did vary over the period of assessment. Recordings were aggregated into integer week values for analysis, thus ensuring that measurement accuracy was not overstated. Two-weekly cohorts were defined to achieve a numerical balance for the determination of leaf age distributions up to week 11. Thereafter, leaves were grouped into a single cohort. As recording did not occur daily, in some cases, only the day by which the leaf had abscinded was measured. In this case the day of leaf death was taken to be the same as the day of abscission. Records of daily maximum and minimum temperatures were obtained from the Long Ashton Research Station meteorological station situated about 1 km from the experimental site. Data for each leaf cohort were analysed to ascertain the extent different clones exhibited variation in the demographic properties of their
al.
leaves. Broadly, data were analysed for (i) differences between clones and cohorts in their rate of production of new leaves; (ii) the rate of death of old leaves, (iii) the survival and longevity of different leaves and (iv) the consequent changes in the age-structure of the leaf canopy population throughout the growing season. Relationships between the above variables and temperature during different parts of the season were analysed. All statistical analyses were made using the GENSTAT 5 statistical package.15 3. RESULTS
3.1. Net changes in leaf number A total of 4118 leaves were sampled during the growing season (1194 for S. x dasyclados, 983 for “Korso” and 1941 for “Mullatin”). The net change in total number of leaves per clone shows that “Mullatin” had a sharper peak than the other two clones, one of which (“Korso”) reached a plateau of about 500 leaves until about day number 250 when the net number of leaves started to decline (Fig. la). There was 1500
a
1
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.*
‘Mullatin’
+
‘Korso’
-
x dasyclados
b 1500
I L u 6
1000
$ z
500
E
0 500
*
‘Mullatm‘
1000 1500 2000 thermal time (oC d above 0 oC)
+
‘Korso’
-
2500
3
x dasyclados
Fig. I. Net number of leaves of three clones of willow as a function of (a) day number and (b) thermal time (“Cd) above a base of 0°C.
Leaf demography in short-rotation Table 1. Mean number of leaves per shoot per replicate plot and clone for Salix x chyclados, “Korso” and “Mullatin” Clone S. x dasyclados “Korso” “Mullatin”
Individual plot means
Clone mean
1
2
3
92.1
87.9
68.8
82.9
63.8 130.2 sed (6 df)
68.3 134.8 7.33
71.0 70.0 129.6 144.6
little difference in this pattern when the same data were plotted on a thermal time scale (Fig. 1b); the effect was simply to lengthen proportionally the plateau phase. The initial rate of increase in leaf number was faster for “Mullatin”, followed by “Korso” and S. x dusycludos (Fig. 1). The rate of decline in net leaf number was fastest for “Mullatin” and slowest for “Korso” (Fig. 1). It is noticeable that the measured onset of the net decline in total leaf number started in all clones on about day number 230 or about 1650”Cd from the start of recording. All clones had lost their leaves by day number 325 or 2780”Cd from the start of growth. The mean number of leaves per shoot differed significantly between clones with “Mullatin” producing the most (p < 0.05) and “Korso” producing the least (Table 1). Mean number of leaves did not differ significantly between “Korso” and S. x dusyclados. 3.2. Leaf production
Leaf cohorts were produced at regular intervals during the season but all clones produced leaves in flushes. Cohorts four and five, tagged on day numbers 132 and 139 respectively, and cohorts 10 and 11, tagged on day numbers 174 and 187, contained substantially more leaves than other cohorts (Fig. 2) although the longer sampling interval between cohorts 10 and 11 inevitably increased the number of leaves per cohort. The mean number of leaves per cohort (Fig. 2) differed little between S. x dusyclados and “Korso” whereas “Mullatin” had an average of about 35% more leaves per cohort than the other clones. The relative birth rate per week (r,,) of leaves into the population was defined as:
321
willow
constant, was fitted to the relative birth rates. By definition, rb has a value of 1 at t = 0 and a minimum value of 0 and the curve was constrained between these limits. Curves for the different clones were not statistically different and the data could be described satisfactorily by a single curve (Fig. 3a) with k = 0.034 (se = 0.0013). 3.3. Leaf death Relative leaf death rates (rd) were calculated for each clone as a function of day number in an analogous way to that for rb, above. The relative death rate (r,J of leaves from the population was defined as: rd = dN,/dt * l/N,
where N, is the total leaf population at time = t. Differences between rd for the different clones became apparent after day number 230. Thereafter, “Korso” had much higher values for rd than the other clones. The progression in relative death rate with time was summarised adequately by a logistic curve (Fig. 3b). From this curve it was possible to calculate the time at which r, = rdmaxas day number 259 for “Korso” and day numbers 313 and 310 for “Mullatin” and S. x dasyclados, respectively. Once r, had started to rise it did so at almost the same rate irrespective of clone. There was no evidence that either the initial asymptote or the maximal rate of change of rd differed between clones (Table 2). 3.4. Leaf longevity and survivorship Leaves from different clones and leaf cohorts lived for different periods irrespective of whether duration was measured in days or thermal time. Leaves of S. burjutica “Korso”
250 ;
rb = dN,/dt . l/N,
where N, is the total leaf population at time = t. From the number of leaves born at each recording time, T,,was calculated for each cohort and clone. A negative exponential curve of the form rb = e( -k’), where k is an exponential rate
Cohort number ‘Mullatin’
m
‘Korso’
x dasyclados
Fig. 2. Number of leaves per cohort for three clones of willow.
J. R. PORTER et al.
328
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Leaf demography in short-rotation Table 2. Parameters of the relative death rate logistic curves of the form
willow
a
x dasvclados
rd = a + (1 - a)/( 1 + exp(-bmaxcr-m))) Parameter
Estimate
se
: m-(5. X aIl.ryclados) M (“Mullatin”) m (“Korso”)
0.0562 0.192 310 313 259
0.0057 0.0183 1.00 0.91 0.72
r, is the relative death rate (on a per week basis), t is the day number and a, b and m are fitted parameters; a is the lower asymptote, b_ the maximum rate of change and m the day number when r, = 0.5( 1 - a). Only the parameter m differs significantly between clones.
04 0
100
50
-
b
time
150 200 day number
1’
250
300
3
thermal time
‘Korao’
__
,lMw)
160,
had a minimum longevity of about 25 days and a maximum longevity of about 65 days, whereas those of S. viminalis “Mullatin” and S. x dasyclados lived for up to 100 days but had similar minimum values to “Korso” (Fig. 4). Measured as thermal time, leaves with the shortest lifespans lived for about 250”Cd for each clone and the longest-lived leaf cohorts of “Korso” lived for about lOOO”Cd, those of “Mullatin” and S. x dasyclados for about 14OO”Cd. The coefficients average of variation (=sd/ mean, expressed as a percentage) for leaf longevity were either almost the same or slightly reduced when leaf duration was expressed in thermal time rather than as number of days for each clone (Table 3). For each clone, the pattern of leaf longevity showed a similar overall form. Leaves born early in the season had similar life-expectancies to those born later. Leaves produced in the middle of the season had the longest lifespans, regardless of clone. Such leaves appeared slightly earlier in “Korso” then in the other clones (Fig. 4). For each replicate plot, the probability of survival for ail leaves was calculated at weekly age-intervals using the Kaplan-Meier estimator of survival for censored data.16 The survivorship curves for the leaves of “Korso” were similar between replicate plots and different from those for the other two clones. The three replicate plots for S. x dasyclados were more similar to each other than were those for “Mullatin” (Fig. Sa). To quantify differences in survivorship both between clones and between leaf cohorts, the time to 50% survival and the difference between the 80th and 20th centiles, i.e. the time from 80% to 20% survival for each clone and leaf
0
s 50
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100
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C
150 200 day number
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358
300
thermal time
‘Mullatin’ lwT---llscc
04 0
50
100
n
150 200 day number
time
250
300
-c
358
thermal time
Fig. 4. Mean longevity, in days or thermal time, of leaf cohorts of (a) Salix x darycfados, (b) “Korso” and (c) “Mullatin” willow clones.
Table 3. The mean coefficients of variation (CV) for leaf longevity in Salk x ahyclados, “Korso” and “Mullatin” when expressed as days or thermal time (“Cd) Clone S. x ahsyclados “Korso” “Mullatin”
Mean CV (%) days 28.8 30.1 60.3
thermal time 28.3 30.8 53.0
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Leaf demography in short-rotation
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331
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Fig. 5. Survivorship data and fitted curves (a), using the Kaplan-Meier estimator, for leaves from three clones of willow, weeks to 50% survival for each cohort (b) and weeks from 80% to 20% survival for each leaf cohort (c).
cohort, was calculated. The time to 50% survival is a measure of the average lifetime, whereas the time from 80% to 20% survival measures the rate of death in the central part of the survivorship curves; the longer the time interval, the slower the death rate. Overall, leaves from “Korso” died at the fastest rates and thus had the shortest average lifetimes (Table 4). No statistically significant difference was found between S. x dasyclados and “Mullatin” in the mean time to 50% survival for the whole leaf population but the mean population from 80% to 20% survival was much shorter for “Mullatin” than for S. x ahsyclados.
The above estimates of survival are for each replicate plot and take no account of the differences that might exist with respect to separate leaf cohorts. Therefore, the above estimates of the time to 50% survival and the time between 80% and 20% survival were calculated separ-
ately for each leaf cohort. In this case, leaf cohort is referred to by the week number of its birth from the start of recording and is not the same as the number of a leaf on a shoot since more than one leaf was produced in a weekly period. All clones showed an increase in the time to 50% survival with increasing cohort number, reaching a maximum value, and then declining (Fig. 5b). The leaf cohort estimated to have the maximum time to 50% survival was cohort 10 for “Korso”, cohort 12 for S. x dasyclados and cohort 13 for “Mullatin”, for which the Table 4. Mean number of days to 50% survival and mean number of days between 80% and 20% survival for all leaves of Salix x dasyclados, “Korso” and “Mullatin” Clone S. x hyclados “Korso” “Mullatin” sed (6 df)
Mean days to 50% survival
Mean days from 80% to 20% survival
82 52 81 4.3
54 24 40 3.3
J. R. PORTERet al.
332
maximum times to 50% survival were 60 days, 96 days and 106 days, respectively. The mean time between 80% and 20% survival for each cohort varied with clone (Fig. 5~). All showed an initial increase in the time between 80% and 20% survival (i.e. a decrease in the rate of death) up to about leaf cohort number six. Thereafter, the 80% to 20% interval for “Korso” increased until leaf cohort 12 whereas, in contrast, it declined for the other two clones. The maximum times from 80% to 20% survival for “Korso”, S. x dasyclados and “Mullatin” were 19 days, 22 days and 33 days, respectively. Figures Sb and 5c also show descriptive curves fitted to these estimates. Time to 50% survival could be described by a quadratic/quadratic function, with a critical exponential function describing the times from 80% to 20% survival. 3.5. Leaf age distribution Differences in relative birth and death rates, and survivorship for leaf cohorts affect the age-structure of the leaf canopy. For these willow clones, the proportion of leaves aged O-10 days throughout the season was similar
780d &
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Fig. 7. Relationship between the absolute rate of leaf production and temperature for three clones of willow. The rate was calculated on a daily basis for each cohort and the mean daily temperature during the production of the particular cohort was used as the independent variable.
between clones (Fig. 6). Naturally, they formed 100% of the population at the start of the season but then progressively declined as a percentage of the population. The only clone with any leaves aged under 10 days at the end of the season was S. x dasyclados. For leaves aged between 11 and 40 days, the age distribution pattern was again similar between clones but also more constant as a proportion of the total leaf population throughout the growing season. Clonal differences in the proportional contribution of age-classes were more apparent for leaves older than 40 days and particularly for leaves older than 60 days: “Korso” had the smallest proportion of leaves in the oldest two age-classes (Fig. 6). It must be remembered that the sample sizes of later cohorts were, by definition, smaller than those for earlier cohorts. Thus, the overall picture of the age structure of the leaf populations through time is of a declining proportion of the youngest leaves, a relatively constant proportion of middle-aged leaves and more variable proportions, both clonally and temporally, for the oldest ones. ture
+ Korso ;
x
20-
3.6. Leaf production: correlation with tempera-
Q**
*
s
s d
$ 250
f, 275
Day number Fig. 6. Change in age-class distribution of leaves with time of three clones of willow.
The rate of leaf production in a variety of temperate and tropical crops has been shown to be positively correlated with temperature (field bean”; sugar beet’*; wheat19; barley”; leeks21*22; groundnut23; millet”). This was also the case for each of the willow clones examined (Fig. 7) for periods during the season when mean temperature was lower than about 14°C. However, above this temperature there was little
Leaf demography in short-rotation
willow
333
Table 5. Parameters of the linear regression of the rate of leaf production (leaves day-‘) on mean temperature for the willow clones, “Korso”, “Mullatin” and Sakx x ahyclados
(4 Slope., m (se) Constant, c I Base temperature (“C)
df
(b) Slope,m (se) Constant, c r
Base temperature (“C)
df
“Korso”
“Mullatin”
S. x ahyclados
1.70 (0.38) -11.64 0.87 6.9 6
2.76 (0.50) - 19.44 0.91 7.0 6
1.59 (0.24) -9.57 0.93 6.0 6
1.14 (1.98) - 10.02 0.20 8.8 7
3.60 (3.10) - 39.59 0.42 11.0 6
1.92 (1.95) -21.21 0.37 11.1 6
The regressions are divided between (a) temperatures < = 14°C and (b) those recorded above this value. Base temperatures are calculated as -c/m.
the effect of the epidemic was not to influence the rate of production of new leaves, or to affect the onset of the decline in net leaf number but to increase substantially the rate of decline in 4. DISCUSSION leaf number once initiated. Similar effects have The functioning of a leaf canopy as an ab- been observed in wheat grown with reduced sorber and utiliser of photosynthetically active levels of nitrogen fertiliser.” The survivorship curves for leaves from each radiation is strongly dependent on the age-structure and position of the leaves that comprise it.13 of the clones correspond to Delvey Type 1 Such information is important for attempts to curves, where the risk of death increases with age in contrast to the other two general types of develop simulation models of canopy growth and function.‘* Also, photosynthetic rate per survivorship where the risk of death is indepenunit leaf area declines with leaf age, with the dent of age (Type 2) or much higher for juvenile decline in the maximum photosynthetic rate stages but lower for adults (Type 3). Type I accounted for by rises in both stomata1 and survivorship patterns have been found for leaf populations of Lolium perenne;8 Linum usitatisinternal resistances to CO, diffusion.14 There were considerable differences in the simum ’ and Pinus nigra.“,” The shape of a survivorship curve is governed change of net number of leaves with time for the three clones of willow investigated (Fig. 1). On by the average lifespan of individuals in the the other hand, there appeared to be many population and the rate of decline in numbers in similarities between the demographic par- the population once death has started. The ameters underpinning the net changes. For average lifespan for any cohort is measured by example, leaves born mid-season had the the time to 50% survival of the cohort and the longest life-spans, regardless of whether time or rate of decline by the time between 80% and thermal time was used as the measure. Leaves 20% survival. Except for the earliest cohorts, produced either at the start or the end of the the time to 50% survival for “Korso” was both season had shorter and similar life-spans consistently and considerably less than for S. x (Fig. 4). The amplitude of the variation in dasyclados or “Mullatin”. The period from 80% longevity was noticeably less for leaves of to 20% survival was lowest in “Korso” until “Korso”. Similarly, little difference was seen leaf cohort 12 but changed its value little for between clones in the relative birth rate of leaves later cohorts. In contrast, S. x dasyclados had the longest period from 80% to 20% survival (Fig. 3a). This was in contrast to the relative death rate which, for “Korso” later in the for leaves until cohort 12 and the shortest period for cohorts 13 and higher. “Mullatin” had, for season, was over three times that of the other two clones (Fig. 3b). With “Korso”, there was the most part, values intermediate between the confounding effect of a severe infection of “Korso” and S. x dasyclados for both time to willow leaf rust caused by Melampsora epitea. 50% survival and the period from 80% to 20% survival. The implications, for the performance From these results it is possible to conclude that
correlation between temperature and leaf production rate for any of the clones (Table 5).
334
J. R. PORTERet al.
of the leaf canopy, of such differences in the underlying configuration of very similar survivorship curves for each clone for the leaf canopy are that, on average, “Korso” maintained a population of predominantly middleaged leaves with relatively fewer older leaves because leaves died earlier. “Mullatin” and S. x dusychdos carried higher proportions of older leaves with all clones holding about the same proportion of the youngest leaves (Fig. 6). In a detailed study of the leaf and ear photosynthesis of winter wheat in the field, the maximum rate of photosynthesis of the penultimate leaves declined from about 30 days after maximum elongation and was zero at 60 days after maximum elongation (see Fig. 8.2 in Marshall14). In cotton, leaf net photosynthetic rate per unit area reached a maximum also after 30 days and then declined monotonically as in wheat.26 In coupling this information with the finding that clonal differences in the mean proportion of leaves per age class start to become apparent for middle to older age classes we conclude that clones which, on average, maintain more juvenile leaf populations may be more productive. Differences in survivorship curves, the time to 50% survival and the relatively short duration of the period from 80% to 20% survival accounted for the net changes in the leaf population of “Korso”. The differences in net leaf number between S. x dasyclados and “Mullatin” were caused by small but important differences in the relative production rates of leaves. The mean value of T,,(on a per day basis) for “Mullatin” for the period during which leaf numbers were increasing was 0.032 (sd = 0.020) whereas that for S. x dasyclados was 0.028 (sd = 0.019). Leaf number continued to rise in both clones until day number 221 and this together with the fact that r, is the parameter in a relationship describing exponential growth explains how supposedly small differences in the value of r, resulted in large differences in final leaf number (Fig. 3). Here, the fact that there were no statistically significant differences between the rd values for the three clones masks the importance of small differences in this parameter. The main finding of this study was the nature of the balance between the demographic features of birth rate, survival rate and death rate of leaves that resulted in the observed leaf population patterns. For “Korso”, the key factor affecting canopy development was the early
onset and rapid death of leaf cohorts. This was a direct result of the heavy incidence of willow leaf rust (Melumpsora epitea) to which “Korso” is very susceptible. There was a clear linear relationship between the rate of leaf production and mean temperature up to 14°C for each of the clones examined. For daily temperatures below a mean of 14°C the base temperatures calculated for each clone were very similar at between 6°C and 7°C (Table 5). Base temperature is that at which the extrapolated rate of a process, in this case leaf production, is zero. However, this relationship held true only for temperatures below about 14°C; base temperatures calculated above this value were higher, less consistent between clones and the degree of correlation between dependent and independent variables was much poorer (Table 5b). Furthermore, the base temperatures for leaf production were much higher than those commonly observed in temperate cereals, where values between 0°C and 2°C have been reported (wheatz7s2*and barley29). The base temperature responses for willow appear more in line with those calculated for maize.30 Interestingly, maize also exhibited an increase in leaf production rate at low temperatures followed by a decline at high temperatures3’ 5. FUTURE
WORK
The data presented in this paper provide one of the bases needed to construct a model of the growth and development of willow shortrotation coppice. Besides the dynamics of canopy development other factors such as the interception of radiation and the partitioning of dry matter between shoots and roots would need to be incorporated.32*33 Such a model, provided it were based on descriptions of the morphological and physiological mechanisms that underpin dry matter production (e.g. Kajfez-Bogataj”) could be used to predict productivities for sites and seasons other than those for which the model was developed. Such a model could also be expanded to include the effects of leaf diseases and nutrition on production from willow short-rotation coppice. Leaf population dynamics are affected by nutrient supply. In Linum usitatissimum, plants provided with complete Long Ashton nutrient solution maintained a persistent leaf canopy for longer than plants in which potassium was excluded from the solution. Here, plants continued to produce leaves for the same period of
Leaf
demographyin short-rotation willow
time but leaves of potassium deficient plants died much sooner. Calcium deficient plants also lost their leaves more quickly than those with a complete complement of nutrients but less quickly than potassium deficient plants.5 HarperI interpreted these differences in terms of the relative mobility of potassium within plants and the relative immobility of calcium. Mobile nutrients will be transferred more readily from older to newer material and thus shorten lifespans more radically than immobile nutrients, a shortage of which reduces the production rate of new material rather than the survival of existing leaves. The effect of different nutritional regimes on canopy development in a semi-perennial such as short rotation willow coppice could be expected to differ from those of an annual plant, because of the availability of mineral nutrients from stem and root reserves. However, studies linking such factors via the demography of leaves and shoots to the photosynthetic rates of leaf canopies are in their infancy (e.g. Alliende3’) and await further experimental and simulation studies. REFERENCES 1. J. L. Monteith, Climate and the efficiency of crop production in Britain. Phil. Trans. Royal Sot. London BUII, 277-294 (1977). 2. J. N. Gallagher and P. V. Biscoe, Radiation, absorption, growth and yield of cereals. J. Agri. Sci., Cambridge 91, 47-60 (I 978). 3. G. Russell, P. G. Jarvis and J. L. Monteith, Absorption of radiation by canopies and stand growth. P/ant Canopies; Their Growth, Form and Function. Societyfor Experimental Biology Seminar Series, 31 (G. Russell,
B. Marshall and P. G. Jarvis, Eds), pp. 21-39. Cambridge University Press, Cambridge (1989). 4. M. G. R. Cannell, R. Mime, L. J. Sheppard and M. H. Unsworth, Radiation interception and-productivity of willow. J. AL&. Ecol. 24. 261-278 (1987). 5. F. A. Bazzaz’and J. L. Harper, Demographic analysis of the growth of Linum usitatissimum. New Phytologist 78, 193-208 (1977). 6. S. C. Clark, Reproductive and vegetative performance in two winter annual grasses, Cafapodium rigidum (L.) C. E. Hubbard and C. murinum (L.) C. E. Hubbard. II.
Leaf demography and its relationship to the production of caryopses. New Phytologist 84, 79-93 (1980). 7. A. H. L. Huiskes and J. L. Harper, The demography of leaves and tillers of Ammophila arenaria in a dune sere. Oecologia Plantarum 14, 435-446 (1979). 8. B. Peters, The demography of leaves in a permanent
pasture. PhD thesis, University of Wales (1980). 9. J. C. Noble, A. D. Bell and J. L. Harper, The popu-
lation biology of plants with clonal growth. I. The morphology-and structural demography of Carex arenaria. J. Ecol. 67. 983-1008 (1979). 10. L. Maillette, Structural dynamics of tree growth with special reference to Betulapendula Roth. and Pinus nigra var maritima (Ait.) Melville. PhD thesis, University of
Wales (1979).
335
L. Maillette, Needle demography and growth dynamics of Corsican Pine. Can. J. Bat. 60. 105-116 (1982). 12. J. R. Porter, A model of canopy development in winter wheat. J. Agr. Sci., Cambridge 102, 383-392 (1984). 13. J. L. Harper, Canopies as populations. Plant Canopies; II.
Their Growth, Form and Function. Society for Experimental Biology Seminar Series, 31 (G. Russell, B.
14.
15.
16. 17
18.
19
Marshall and P. G. Jarvis, Eds), pp. 105-128. Cambridge University Press, Cambridge. B. Marshall, Leaf and ear photosynthesis of winter wheat crops. PhD thesis, University of Nottingham (1978). R. W. Payne, P. W. Lane, A. E. Ainsley, K. E. Bicknell, P. G. N. Digby, S. A. Harding, P. K. Leech, H. R. Simpson, A. D. Todd, P. J. Verrier, R. P. White, J. C. Gower, G. Tunicliffe-Wilson and L. J. Paterson, Gensfat 5 Reference Manual. Oxford University Press, Oxford (1987). D. R. Cox and D. Oakes, Analysis of Survival Data. Chapman and Hall, London (1984). M. D. Dennett, J. Elston and J. R. Milford, The effects of temperature on the growth of individual leaves of Viciafaba L. in the field. Annals Bat. 43, 197-208 (1979). G. F. J. Milford, T. 0. Pocock and J. Riley, An analysis of leaf growth in sugar beet. 2. Leaf appearance in field crops. Annals Appl.-Biol. 106, 173-185 (1985). C. K. Baker. J. N. Gallagher and J. L. Monteith. Daylength change and leaf appearance in winter wheat. Plant Cell Environ. 3, 285-287 (1980).
20. E. J. M. Kirby, M. Appleyard and G. Feilowes, Effect of sowing date and variety on main shoot leaf emergence and number of leaves of barley and wheat. Agronomie, 5, 117-126 (1985).
21. R. K. M. Hay and J. R. Brown, Field studies of leaf development and expansion in the leek (Allium porrum). Annals Appl. Biol. 113, 617-625
(1988).
22. R. K. M. Hay and D. R. Kemp, The prediction of leaf canopy expansion in the leek from a simple model dependent on primordial development. Annals Appl. Biol. 120, (in press) (1992). 23. S. K. Leong and C. K. Ong, The influence of temperature and soil water deficit on the development and morphology of groundnut (Arachir hypogea L.). J. Exp. Botany 34, 1551-1561.
24. C. K. Ong, Response to temperature in a stand of pearl millet (Pennisetum ryphoides S. and H.). I. Vegetative development. J. Exp. Bor. 34, 322-336 (1983). 25. V. B. A. Willington and P. V. Biscoe, Growth and Development of Winter Wheat. Brooms Barn Experimental Station, Bury St Edmunds (1983). 26. G. A. Constable and H. M. Rawson. Effect of leaf position, expansion and age on photosynthesis, transpiration and water use efficiency of cotton. Alcsr. J. Planr Physiol. 7, 899100 (1980).
27. E. J. M. Kirby, J. R. Porter, W. Day, J. S. Adam, M. Appleyard, S. Ayling, C. K. Baker, R. K. Belford, P. V. Biscoe, A. Chapman, M. P. Fuller, J. Hampson, R. K. M. Hay, S. Matthews, W. J. Thompson, A. H. Weir, V. B. A. Willington and D. W. Wood, An analysis of primordium initiation in Avalon winter wheat crops with different sowing dates and at nine sites in England and Scotland. J. Agri. Sci. Cambridge 109, 123-134 (1987).
28. E. J. M. Kirby, A field study of the number of main shoot leaves in wheat in relation to vernalisation and photoperiod. J. Agri. Sci., Cambridge 118, 271-278 (1992).
29. E. J. M. Kirby, M. Appleyard and G. Fellowes, Effect of sowing date on the temperature response of leaf emergence and leaf size in barley. PIam Cell Enuiron. 5, 477-484
(1982).
30 I. J. Warrington and E. T. Kanemasu, Corn growth response to temperature and photoperiod. II. Leaf-
336
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initiation and leaf appearance rates. Agronomy J. 75, 755-761 (1983a). 31. I. J. Warrington and E. T. Kanemasu, Corn growth response to temperature and photoperiod. III. Leaf number. Agronomy J. 75, 762-766 (1983b). 32. H. van Keulan and J. Wolf, Modeliing of Agricultural Production: Weather, Soils and Crops. Pudoc, Wageningen (1986). 33. H. Eckersten, A. Lindroth and L.-O. Nilsson, Simulated growth of willow stands related to variations in weather
content. Modelling of Energy Forestry: Growth, Water Relations and Economics (K. L.
and foliar nitrogen
Perttu and P. J. Kowalik, Eds), pp. 33-63. Pudoc, Wageningen (1989). 34. L. Kajfez-Bogataj, Photosynthetic model for predicting net willow stand production. Agr. Forest Meteorol. SO, 75-85. (1990). 35. M. C. Alliende, Growth and reproduction in a dioecious tree, Salk cinerea. PhD thesis, University of Wales (1986).
0961-9534/93 56.00+O.OO
Biomass and Bioenergy
LEAF DEMOGRAPHY
0 1993Pergamon Press Ltd
IN WILLOW SHORT-ROTATION COPPICE
JOHNR. PORTER, RODNEY I. PARFITTand GILLIANM. ARNOLD Department of Agricultural Sciences, University of Bristol, AFRC Institute of Arable Crops Research, Long Ashton Research Station, Bristol, BS18 9AF, U.K. (Received 28 May 1993; accepted
13 August 1993)
Abstract-The production, survivorship and death of cohorts of leaves within the canopies of three clones (Sulix burjatica “Korso”, S. viminnlis “Mullatin” and S. x dnsyclados) of willow grown as short-rotation coppice were studied in a field experiment. The initial rate of increase in leaf number was fastest for “Mullatin”, which also had the steepest rate of decline in net leaf number. Inter-clonal variability was not reduced by plotting changes in leaf number against thermal time, accumulated above 0°C. Mean number of leaves was highest for “Mullatin” and least for “Korso”. Leaf production occurred in flushes and there were no significant clonal differences in the relative rate of leaf birth: differences in relative rate of leaf death (r,,) became apparent after day number 230 (1 Jan = 1); thereafter “Korso” had higher values of r, than the other clones. The time course of r, was summarked by a logistic curve and there was no evidence that the initial asymptote nor the maximal rate of change of r, differed between clones. Leaves of “Korso” had minimum and maximum longevities of about 25 days (or about 2SO”Cd in thermal time) and 65 days (about IOOO‘Cd),respectively; minimum leaf longevities for the other two clones were similar to that for “Korso” but their leaves lived for up to 100 days (about 14OOCd). Changes in the age-structure of the leaf populations with time were little influenced by differences in leaf demography between clones. A positive and significant correlation was found between the rate of production of leaves and temperature up to about 14°C. Thereafter, the correlation was either absent or negative. Results are interpreted in terms of the consequences of differences in canopy demography for coppice biomass production. Keywords-Canopy,
coppice, demography, leaves, willow.
1. INTRODUCTION
Previous work has shown that the dry matter productivity of many crops is related linearly to the quantity of photosynthetically active radiThis is also the case with ation they absorb. ‘*2*3 willows grown as a short-rotation crop and coppiced on a four-to-five year cycle.4 This relationship depends both on the efficiency of absorption of radiation per unit time and the duration of interception. Both processes are influenced by the architectural form of the leaf canopy of which an important determinant is the age-structure and population dynamics of shoots and leaves. Demographic studies of leaves and shoots have been made for Linum usitatissimum,’ Catapodium ~pp.,~ Ammophila arenaria,’ Lolium perenne,’ Carex arenaria 9 and Betula pendula and Pinus nigra.“,” Models of
canopy development based explicitly on the demographic behaviour of shoots and leaves have been developed for cereals.12
The photosynthetic activity of a canopy depends on the age-structure of its component leaves.13 MarshallI showed that the maximum rate of photosynthesis declined monotonically with age for the flag and penultimate leaves of wheat. Whereas stomata1 resistance did not increase greatly with leaf age, increases in mesophyll and carboxylation resistances to CO2 incorporation were found. Thus, in order to predict the dry matter production of a stand of willows or other perennial vegetation, knowledge of the demography of the leaf canopy is required. This study investigates the population dynamics of leaf populations of three clones of willow used in short-rotation coppice. The clones were chosen because they exhibit wide variation in their architectural form and because they are important varieties for biomass production. The study also links demographic parameters such as leaf birth and death rates to temperature. The consequences of differences 325
J. R. PORTERet
326
in the population dynamics of the leaf canopy for the age-structure, and by implication the efficiency of the canopy, are also assessed. 2. MATERIALS
AND METHODS
The production, survival and death of leaves on three clones of willow were censused from spring until autumn 1988 at Long Ashton Research Station, Bristol, U.K. (latitude 50.5”N). The clones chosen for study were Salix burjatica “Korso”, S. viminalis “Mullatin” and S. x dasyclados. At each census every fifth leaf, on selected shoots, in the group of leaves produced since the previous sampling was identified and tagged with differently coloured, non-toxic plastic tape. The complete group of leaves formed a cohort of leaves from which each fifth leaf was non-destructively and successively sampled throughout its lifetime. Measurements were taken from three replicate single clonal plots for each clone with 12 plants per replicate plot and two shoots were sampled per plant, chosen at random. Data were recorded for each sample leaf on a hand-held data logger (Epson HX-20) from which the results were passed to a mainframe computer for analysis. Leaf demographic measurement started on 18 April 1988 (day number 109) and continued until 21 November 1988 (day number 325). During this period there were 25 dates, at approximately weekly intervals, during which samples of leaves were assessed as being either living, dead but still attached to the shoot or dead and abscinded from the shoot. Although the sampling interval was approximately weekly, this did vary over the period of assessment. Recordings were aggregated into integer week values for analysis, thus ensuring that measurement accuracy was not overstated. Two-weekly cohorts were defined to achieve a numerical balance for the determination of leaf age distributions up to week 11. Thereafter, leaves were grouped into a single cohort. As recording did not occur daily, in some cases, only the day by which the leaf had abscinded was measured. In this case the day of leaf death was taken to be the same as the day of abscission. Records of daily maximum and minimum temperatures were obtained from the Long Ashton Research Station meteorological station situated about 1 km from the experimental site. Data for each leaf cohort were analysed to ascertain the extent different clones exhibited variation in the demographic properties of their
al.
leaves. Broadly, data were analysed for (i) differences between clones and cohorts in their rate of production of new leaves; (ii) the rate of death of old leaves, (iii) the survival and longevity of different leaves and (iv) the consequent changes in the age-structure of the leaf canopy population throughout the growing season. Relationships between the above variables and temperature during different parts of the season were analysed. All statistical analyses were made using the GENSTAT 5 statistical package.15 3. RESULTS
3.1. Net changes in leaf number A total of 4118 leaves were sampled during the growing season (1194 for S. x dasyclados, 983 for “Korso” and 1941 for “Mullatin”). The net change in total number of leaves per clone shows that “Mullatin” had a sharper peak than the other two clones, one of which (“Korso”) reached a plateau of about 500 leaves until about day number 250 when the net number of leaves started to decline (Fig. la). There was 1500
a
1
O-
.*
‘Mullatin’
+
‘Korso’
-
x dasyclados
b 1500
I L u 6
1000
$ z
500
E
0 500
*
‘Mullatm‘
1000 1500 2000 thermal time (oC d above 0 oC)
+
‘Korso’
-
2500
3
x dasyclados
Fig. I. Net number of leaves of three clones of willow as a function of (a) day number and (b) thermal time (“Cd) above a base of 0°C.
Leaf demography in short-rotation Table 1. Mean number of leaves per shoot per replicate plot and clone for Salix x chyclados, “Korso” and “Mullatin” Clone S. x dasyclados “Korso” “Mullatin”
Individual plot means
Clone mean
1
2
3
92.1
87.9
68.8
82.9
63.8 130.2 sed (6 df)
68.3 134.8 7.33
71.0 70.0 129.6 144.6
little difference in this pattern when the same data were plotted on a thermal time scale (Fig. 1b); the effect was simply to lengthen proportionally the plateau phase. The initial rate of increase in leaf number was faster for “Mullatin”, followed by “Korso” and S. x dusycludos (Fig. 1). The rate of decline in net leaf number was fastest for “Mullatin” and slowest for “Korso” (Fig. 1). It is noticeable that the measured onset of the net decline in total leaf number started in all clones on about day number 230 or about 1650”Cd from the start of recording. All clones had lost their leaves by day number 325 or 2780”Cd from the start of growth. The mean number of leaves per shoot differed significantly between clones with “Mullatin” producing the most (p < 0.05) and “Korso” producing the least (Table 1). Mean number of leaves did not differ significantly between “Korso” and S. x dusyclados. 3.2. Leaf production
Leaf cohorts were produced at regular intervals during the season but all clones produced leaves in flushes. Cohorts four and five, tagged on day numbers 132 and 139 respectively, and cohorts 10 and 11, tagged on day numbers 174 and 187, contained substantially more leaves than other cohorts (Fig. 2) although the longer sampling interval between cohorts 10 and 11 inevitably increased the number of leaves per cohort. The mean number of leaves per cohort (Fig. 2) differed little between S. x dusyclados and “Korso” whereas “Mullatin” had an average of about 35% more leaves per cohort than the other clones. The relative birth rate per week (r,,) of leaves into the population was defined as:
321
willow
constant, was fitted to the relative birth rates. By definition, rb has a value of 1 at t = 0 and a minimum value of 0 and the curve was constrained between these limits. Curves for the different clones were not statistically different and the data could be described satisfactorily by a single curve (Fig. 3a) with k = 0.034 (se = 0.0013). 3.3. Leaf death Relative leaf death rates (rd) were calculated for each clone as a function of day number in an analogous way to that for rb, above. The relative death rate (r,J of leaves from the population was defined as: rd = dN,/dt * l/N,
where N, is the total leaf population at time = t. Differences between rd for the different clones became apparent after day number 230. Thereafter, “Korso” had much higher values for rd than the other clones. The progression in relative death rate with time was summarised adequately by a logistic curve (Fig. 3b). From this curve it was possible to calculate the time at which r, = rdmaxas day number 259 for “Korso” and day numbers 313 and 310 for “Mullatin” and S. x dasyclados, respectively. Once r, had started to rise it did so at almost the same rate irrespective of clone. There was no evidence that either the initial asymptote or the maximal rate of change of rd differed between clones (Table 2). 3.4. Leaf longevity and survivorship Leaves from different clones and leaf cohorts lived for different periods irrespective of whether duration was measured in days or thermal time. Leaves of S. burjutica “Korso”
250 ;
rb = dN,/dt . l/N,
where N, is the total leaf population at time = t. From the number of leaves born at each recording time, T,,was calculated for each cohort and clone. A negative exponential curve of the form rb = e( -k’), where k is an exponential rate
Cohort number ‘Mullatin’
m
‘Korso’
x dasyclados
Fig. 2. Number of leaves per cohort for three clones of willow.
J. R. PORTER et al.
328
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Leaf demography in short-rotation Table 2. Parameters of the relative death rate logistic curves of the form
willow
a
x dasvclados
rd = a + (1 - a)/( 1 + exp(-bmaxcr-m))) Parameter
Estimate
se
: m-(5. X aIl.ryclados) M (“Mullatin”) m (“Korso”)
0.0562 0.192 310 313 259
0.0057 0.0183 1.00 0.91 0.72
r, is the relative death rate (on a per week basis), t is the day number and a, b and m are fitted parameters; a is the lower asymptote, b_ the maximum rate of change and m the day number when r, = 0.5( 1 - a). Only the parameter m differs significantly between clones.
04 0
100
50
-
b
time
150 200 day number
1’
250
300
3
thermal time
‘Korao’
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160,
had a minimum longevity of about 25 days and a maximum longevity of about 65 days, whereas those of S. viminalis “Mullatin” and S. x dasyclados lived for up to 100 days but had similar minimum values to “Korso” (Fig. 4). Measured as thermal time, leaves with the shortest lifespans lived for about 250”Cd for each clone and the longest-lived leaf cohorts of “Korso” lived for about lOOO”Cd, those of “Mullatin” and S. x dasyclados for about 14OO”Cd. The coefficients average of variation (=sd/ mean, expressed as a percentage) for leaf longevity were either almost the same or slightly reduced when leaf duration was expressed in thermal time rather than as number of days for each clone (Table 3). For each clone, the pattern of leaf longevity showed a similar overall form. Leaves born early in the season had similar life-expectancies to those born later. Leaves produced in the middle of the season had the longest lifespans, regardless of clone. Such leaves appeared slightly earlier in “Korso” then in the other clones (Fig. 4). For each replicate plot, the probability of survival for ail leaves was calculated at weekly age-intervals using the Kaplan-Meier estimator of survival for censored data.16 The survivorship curves for the leaves of “Korso” were similar between replicate plots and different from those for the other two clones. The three replicate plots for S. x dasyclados were more similar to each other than were those for “Mullatin” (Fig. Sa). To quantify differences in survivorship both between clones and between leaf cohorts, the time to 50% survival and the difference between the 80th and 20th centiles, i.e. the time from 80% to 20% survival for each clone and leaf
0
s 50
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n
time
C
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358
300
thermal time
‘Mullatin’ lwT---llscc
04 0
50
100
n
150 200 day number
time
250
300
-c
358
thermal time
Fig. 4. Mean longevity, in days or thermal time, of leaf cohorts of (a) Salix x darycfados, (b) “Korso” and (c) “Mullatin” willow clones.
Table 3. The mean coefficients of variation (CV) for leaf longevity in Salk x ahyclados, “Korso” and “Mullatin” when expressed as days or thermal time (“Cd) Clone S. x ahsyclados “Korso” “Mullatin”
Mean CV (%) days 28.8 30.1 60.3
thermal time 28.3 30.8 53.0
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Leaf demography in short-rotation
I
I
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331
I
0
20
24
1
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+-+
t
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Fig. 5. Survivorship data and fitted curves (a), using the Kaplan-Meier estimator, for leaves from three clones of willow, weeks to 50% survival for each cohort (b) and weeks from 80% to 20% survival for each leaf cohort (c).
cohort, was calculated. The time to 50% survival is a measure of the average lifetime, whereas the time from 80% to 20% survival measures the rate of death in the central part of the survivorship curves; the longer the time interval, the slower the death rate. Overall, leaves from “Korso” died at the fastest rates and thus had the shortest average lifetimes (Table 4). No statistically significant difference was found between S. x dasyclados and “Mullatin” in the mean time to 50% survival for the whole leaf population but the mean population from 80% to 20% survival was much shorter for “Mullatin” than for S. x ahsyclados.
The above estimates of survival are for each replicate plot and take no account of the differences that might exist with respect to separate leaf cohorts. Therefore, the above estimates of the time to 50% survival and the time between 80% and 20% survival were calculated separ-
ately for each leaf cohort. In this case, leaf cohort is referred to by the week number of its birth from the start of recording and is not the same as the number of a leaf on a shoot since more than one leaf was produced in a weekly period. All clones showed an increase in the time to 50% survival with increasing cohort number, reaching a maximum value, and then declining (Fig. 5b). The leaf cohort estimated to have the maximum time to 50% survival was cohort 10 for “Korso”, cohort 12 for S. x dasyclados and cohort 13 for “Mullatin”, for which the Table 4. Mean number of days to 50% survival and mean number of days between 80% and 20% survival for all leaves of Salix x dasyclados, “Korso” and “Mullatin” Clone S. x hyclados “Korso” “Mullatin” sed (6 df)
Mean days to 50% survival
Mean days from 80% to 20% survival
82 52 81 4.3
54 24 40 3.3
J. R. PORTERet al.
332
maximum times to 50% survival were 60 days, 96 days and 106 days, respectively. The mean time between 80% and 20% survival for each cohort varied with clone (Fig. 5~). All showed an initial increase in the time between 80% and 20% survival (i.e. a decrease in the rate of death) up to about leaf cohort number six. Thereafter, the 80% to 20% interval for “Korso” increased until leaf cohort 12 whereas, in contrast, it declined for the other two clones. The maximum times from 80% to 20% survival for “Korso”, S. x dasyclados and “Mullatin” were 19 days, 22 days and 33 days, respectively. Figures Sb and 5c also show descriptive curves fitted to these estimates. Time to 50% survival could be described by a quadratic/quadratic function, with a critical exponential function describing the times from 80% to 20% survival. 3.5. Leaf age distribution Differences in relative birth and death rates, and survivorship for leaf cohorts affect the age-structure of the leaf canopy. For these willow clones, the proportion of leaves aged O-10 days throughout the season was similar
780d &
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*
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x
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Fig. 7. Relationship between the absolute rate of leaf production and temperature for three clones of willow. The rate was calculated on a daily basis for each cohort and the mean daily temperature during the production of the particular cohort was used as the independent variable.
between clones (Fig. 6). Naturally, they formed 100% of the population at the start of the season but then progressively declined as a percentage of the population. The only clone with any leaves aged under 10 days at the end of the season was S. x dasyclados. For leaves aged between 11 and 40 days, the age distribution pattern was again similar between clones but also more constant as a proportion of the total leaf population throughout the growing season. Clonal differences in the proportional contribution of age-classes were more apparent for leaves older than 40 days and particularly for leaves older than 60 days: “Korso” had the smallest proportion of leaves in the oldest two age-classes (Fig. 6). It must be remembered that the sample sizes of later cohorts were, by definition, smaller than those for earlier cohorts. Thus, the overall picture of the age structure of the leaf populations through time is of a declining proportion of the youngest leaves, a relatively constant proportion of middle-aged leaves and more variable proportions, both clonally and temporally, for the oldest ones. ture
+ Korso ;
x
20-
3.6. Leaf production: correlation with tempera-
Q**
*
s
s d
$ 250
f, 275
Day number Fig. 6. Change in age-class distribution of leaves with time of three clones of willow.
The rate of leaf production in a variety of temperate and tropical crops has been shown to be positively correlated with temperature (field bean”; sugar beet’*; wheat19; barley”; leeks21*22; groundnut23; millet”). This was also the case for each of the willow clones examined (Fig. 7) for periods during the season when mean temperature was lower than about 14°C. However, above this temperature there was little
Leaf demography in short-rotation
willow
333
Table 5. Parameters of the linear regression of the rate of leaf production (leaves day-‘) on mean temperature for the willow clones, “Korso”, “Mullatin” and Sakx x ahyclados
(4 Slope., m (se) Constant, c I Base temperature (“C)
df
(b) Slope,m (se) Constant, c r
Base temperature (“C)
df
“Korso”
“Mullatin”
S. x ahyclados
1.70 (0.38) -11.64 0.87 6.9 6
2.76 (0.50) - 19.44 0.91 7.0 6
1.59 (0.24) -9.57 0.93 6.0 6
1.14 (1.98) - 10.02 0.20 8.8 7
3.60 (3.10) - 39.59 0.42 11.0 6
1.92 (1.95) -21.21 0.37 11.1 6
The regressions are divided between (a) temperatures < = 14°C and (b) those recorded above this value. Base temperatures are calculated as -c/m.
the effect of the epidemic was not to influence the rate of production of new leaves, or to affect the onset of the decline in net leaf number but to increase substantially the rate of decline in 4. DISCUSSION leaf number once initiated. Similar effects have The functioning of a leaf canopy as an ab- been observed in wheat grown with reduced sorber and utiliser of photosynthetically active levels of nitrogen fertiliser.” The survivorship curves for leaves from each radiation is strongly dependent on the age-structure and position of the leaves that comprise it.13 of the clones correspond to Delvey Type 1 Such information is important for attempts to curves, where the risk of death increases with age in contrast to the other two general types of develop simulation models of canopy growth and function.‘* Also, photosynthetic rate per survivorship where the risk of death is indepenunit leaf area declines with leaf age, with the dent of age (Type 2) or much higher for juvenile decline in the maximum photosynthetic rate stages but lower for adults (Type 3). Type I accounted for by rises in both stomata1 and survivorship patterns have been found for leaf populations of Lolium perenne;8 Linum usitatisinternal resistances to CO, diffusion.14 There were considerable differences in the simum ’ and Pinus nigra.“,” The shape of a survivorship curve is governed change of net number of leaves with time for the three clones of willow investigated (Fig. 1). On by the average lifespan of individuals in the the other hand, there appeared to be many population and the rate of decline in numbers in similarities between the demographic par- the population once death has started. The ameters underpinning the net changes. For average lifespan for any cohort is measured by example, leaves born mid-season had the the time to 50% survival of the cohort and the longest life-spans, regardless of whether time or rate of decline by the time between 80% and thermal time was used as the measure. Leaves 20% survival. Except for the earliest cohorts, produced either at the start or the end of the the time to 50% survival for “Korso” was both season had shorter and similar life-spans consistently and considerably less than for S. x (Fig. 4). The amplitude of the variation in dasyclados or “Mullatin”. The period from 80% longevity was noticeably less for leaves of to 20% survival was lowest in “Korso” until “Korso”. Similarly, little difference was seen leaf cohort 12 but changed its value little for between clones in the relative birth rate of leaves later cohorts. In contrast, S. x dasyclados had the longest period from 80% to 20% survival (Fig. 3a). This was in contrast to the relative death rate which, for “Korso” later in the for leaves until cohort 12 and the shortest period for cohorts 13 and higher. “Mullatin” had, for season, was over three times that of the other two clones (Fig. 3b). With “Korso”, there was the most part, values intermediate between the confounding effect of a severe infection of “Korso” and S. x dasyclados for both time to willow leaf rust caused by Melampsora epitea. 50% survival and the period from 80% to 20% survival. The implications, for the performance From these results it is possible to conclude that
correlation between temperature and leaf production rate for any of the clones (Table 5).
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of the leaf canopy, of such differences in the underlying configuration of very similar survivorship curves for each clone for the leaf canopy are that, on average, “Korso” maintained a population of predominantly middleaged leaves with relatively fewer older leaves because leaves died earlier. “Mullatin” and S. x dusychdos carried higher proportions of older leaves with all clones holding about the same proportion of the youngest leaves (Fig. 6). In a detailed study of the leaf and ear photosynthesis of winter wheat in the field, the maximum rate of photosynthesis of the penultimate leaves declined from about 30 days after maximum elongation and was zero at 60 days after maximum elongation (see Fig. 8.2 in Marshall14). In cotton, leaf net photosynthetic rate per unit area reached a maximum also after 30 days and then declined monotonically as in wheat.26 In coupling this information with the finding that clonal differences in the mean proportion of leaves per age class start to become apparent for middle to older age classes we conclude that clones which, on average, maintain more juvenile leaf populations may be more productive. Differences in survivorship curves, the time to 50% survival and the relatively short duration of the period from 80% to 20% survival accounted for the net changes in the leaf population of “Korso”. The differences in net leaf number between S. x dasyclados and “Mullatin” were caused by small but important differences in the relative production rates of leaves. The mean value of T,,(on a per day basis) for “Mullatin” for the period during which leaf numbers were increasing was 0.032 (sd = 0.020) whereas that for S. x dasyclados was 0.028 (sd = 0.019). Leaf number continued to rise in both clones until day number 221 and this together with the fact that r, is the parameter in a relationship describing exponential growth explains how supposedly small differences in the value of r, resulted in large differences in final leaf number (Fig. 3). Here, the fact that there were no statistically significant differences between the rd values for the three clones masks the importance of small differences in this parameter. The main finding of this study was the nature of the balance between the demographic features of birth rate, survival rate and death rate of leaves that resulted in the observed leaf population patterns. For “Korso”, the key factor affecting canopy development was the early
onset and rapid death of leaf cohorts. This was a direct result of the heavy incidence of willow leaf rust (Melumpsora epitea) to which “Korso” is very susceptible. There was a clear linear relationship between the rate of leaf production and mean temperature up to 14°C for each of the clones examined. For daily temperatures below a mean of 14°C the base temperatures calculated for each clone were very similar at between 6°C and 7°C (Table 5). Base temperature is that at which the extrapolated rate of a process, in this case leaf production, is zero. However, this relationship held true only for temperatures below about 14°C; base temperatures calculated above this value were higher, less consistent between clones and the degree of correlation between dependent and independent variables was much poorer (Table 5b). Furthermore, the base temperatures for leaf production were much higher than those commonly observed in temperate cereals, where values between 0°C and 2°C have been reported (wheatz7s2*and barley29). The base temperature responses for willow appear more in line with those calculated for maize.30 Interestingly, maize also exhibited an increase in leaf production rate at low temperatures followed by a decline at high temperatures3’ 5. FUTURE
WORK
The data presented in this paper provide one of the bases needed to construct a model of the growth and development of willow shortrotation coppice. Besides the dynamics of canopy development other factors such as the interception of radiation and the partitioning of dry matter between shoots and roots would need to be incorporated.32*33 Such a model, provided it were based on descriptions of the morphological and physiological mechanisms that underpin dry matter production (e.g. Kajfez-Bogataj”) could be used to predict productivities for sites and seasons other than those for which the model was developed. Such a model could also be expanded to include the effects of leaf diseases and nutrition on production from willow short-rotation coppice. Leaf population dynamics are affected by nutrient supply. In Linum usitatissimum, plants provided with complete Long Ashton nutrient solution maintained a persistent leaf canopy for longer than plants in which potassium was excluded from the solution. Here, plants continued to produce leaves for the same period of
Leaf
demographyin short-rotation willow
time but leaves of potassium deficient plants died much sooner. Calcium deficient plants also lost their leaves more quickly than those with a complete complement of nutrients but less quickly than potassium deficient plants.5 HarperI interpreted these differences in terms of the relative mobility of potassium within plants and the relative immobility of calcium. Mobile nutrients will be transferred more readily from older to newer material and thus shorten lifespans more radically than immobile nutrients, a shortage of which reduces the production rate of new material rather than the survival of existing leaves. The effect of different nutritional regimes on canopy development in a semi-perennial such as short rotation willow coppice could be expected to differ from those of an annual plant, because of the availability of mineral nutrients from stem and root reserves. However, studies linking such factors via the demography of leaves and shoots to the photosynthetic rates of leaf canopies are in their infancy (e.g. Alliende3’) and await further experimental and simulation studies. REFERENCES 1. J. L. Monteith, Climate and the efficiency of crop production in Britain. Phil. Trans. Royal Sot. London BUII, 277-294 (1977). 2. J. N. Gallagher and P. V. Biscoe, Radiation, absorption, growth and yield of cereals. J. Agri. Sci., Cambridge 91, 47-60 (I 978). 3. G. Russell, P. G. Jarvis and J. L. Monteith, Absorption of radiation by canopies and stand growth. P/ant Canopies; Their Growth, Form and Function. Societyfor Experimental Biology Seminar Series, 31 (G. Russell,
B. Marshall and P. G. Jarvis, Eds), pp. 21-39. Cambridge University Press, Cambridge (1989). 4. M. G. R. Cannell, R. Mime, L. J. Sheppard and M. H. Unsworth, Radiation interception and-productivity of willow. J. AL&. Ecol. 24. 261-278 (1987). 5. F. A. Bazzaz’and J. L. Harper, Demographic analysis of the growth of Linum usitatissimum. New Phytologist 78, 193-208 (1977). 6. S. C. Clark, Reproductive and vegetative performance in two winter annual grasses, Cafapodium rigidum (L.) C. E. Hubbard and C. murinum (L.) C. E. Hubbard. II.
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