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9 Springer-Verlag 1987. Respiration and photosynthesis in cones of Norway spruce. (P 'cea abies (L.) Karst.) Andres Koppel*, Erik Troeng, and Sune Linder.
Trees (1987) 1:123-128 9 Springer-Verlag 1987

Respiration and photosynthesis in cones of Norway spruce (P 'cea abies (L.) Karst.) Andres Koppel*, Erik Troeng, and Sune Linder Swedish University of Agricultural Sciences, Department of Ecology and Environmental Research P. O. Box 7072, S-75007 Uppsala, Sweden

Summary. Dark respiration and photosynthetic carbon dioxide refixation in purple and green Picea abies cones were investigated from budbreak to cone maturity. The rate of dark respiration per unit dry weight and CO2 refixation capacity decreased during cone maturation. At the beginning of the growing season, photosynthetic CO 2 refixation could reduce the amount of CO 2 released by respiration in green and purple cones by 50% and 40%, respectively. The seasonal performance of the components of the cone carbon balance was calculated using information on the seasonal course of respiration, refixation capacity and the light response curves of cone photosynthesis, as well as the actual light and temperature regime in the field. The daily gain of CO 2 refixation reached 28%-34% of respiration in green and 22%-26% in purple cones during the first month of their growth, but decreased later in the season. Over the entire growth period refixation reduced carbon costs of cone production in both cone colour polymorphs by 16%- 17%. Key words: Carbon balance - Cones - Photosynthetic CO 2 refixation - Picea abies - Respiration - Seasonal course

Introduction

A considerable part of the annual photosynthetic production in conifers is used in cone and seed production. This can reduce both height growth * Permanent address: Laboratory of Ecosystems, Tartu State University, 18 Ulikooli St., 202400 Tartu, Estonian SSR, USSR Offprint requests to: S. Linder

(Teich 1975) and radial stem increment (Eis et al. 1965). Based on growth ring analysis, increment losses in Norway spruce caused by cone production have been reported to be between 12% and 40% (e.g. Danilov 1953; Buyak 1975; Chalupka et al. 1975), and Rohmeder (1967) estimated that as much as 150 m 3 ha -I of potential stemwood production was lost over one rotation. In addition to these indirect estimates of cone crop effects on stem growth, the metabolic costs of cone production may be investigated by studying the carbon balance. Linder and Troeng (1981 a) measured growth, respiration and carbon dioxide refixation throughout the life cycle of cones in Scots pine and were able to estimate a carbon budget for cone production. According to their estimates, cone production could equal 10%-15% of stemwood production during an average year. They also reported a considerable photosynthetic refixation of carbon dioxide released by cone respiration. Of the respired carbon dioxide 31% was refixed, thus contributing appreciably to the carbon economy of the tree. Bazzaz et al. (1979) determined the carbon budget for reproduction and the contribution of fruit and flower photosynthesis in 15 temperate deciduous trees. They showed that photosynthesis by reproductive organs was common and contributed a considerable part of the total carbon balance in fruits. Thus in Acer platanoides, refixation supplied 64.5% of the total carbon required for fruit production, and in Betula pendula the amount was 21.7%. In Norway spruce, cone coloration varies from bright green to dark purple (Dallimore and Jackson 1966; Schmidt-Vogt 1986). Individual trees produce cones with the same colour through-

124

out their life. The intensity of purple coloration depends somewhat however on exposure to direct sunlight, shaded cones being less pigmented (Etverk 1965). Purple cones mature earlier than green cones; in German the two types are known as "early spruce" and "late spruce". The proportion of purple cones increases in the northern parts of the Norway spruce distribution area and at higher altitudes (Etverk 1965; Schmidt-Vogt 1987). Since no obvious correlation between cone coloration and stem growth has been observed, interest in this phenomenon in forestry has been small (Etverk 1965). Very few attempts have been made to estimate the adaptational value of different cone coloration. Sturgeon and Mitton (1980) measured higher temperature in sunlit purple cones than in green cones of Abies concolor and suggested the possible advantages of a higher temperature at sites with short and cold summers. Kozubov (1962) measured a higher temperature sum in red than in green strobili of Pinus sylvestris. The aim of this study was to evaluate the components of the carbon economy, dark respiration and CO 2 refixation in green and purple cone polymorphs of Norway spruce throughout the growth period of the cones. Material and methods Sample trees. Two mature Norway spruce trees, distinctly different in cone coloration, growing in the vicinity of J~idrahs Ecological Research Station, Central Sweden (60~ ' N, 16030 ' E, altitude 180 m above sea level) were chosen. The height of the sample trees was approximately 20 m and the age about 140 years. The cones were sampled from the southern side of the crowns from 17 May until 23 September. This period covered most of the time from budbreak of shoots to cone maturity (defined by a water content 1 m s -~) assimilation chamber.

Table 1. The change in cone respiration after detachment (percentage of the initial value) with and without water supply. The measurements were at 20~ Time after detachment (h)

With water Without water

10

20

40

97 79

91 59

47 37

The cylindrical assimilation chamber consisted of a brass tube with a perspex window at the upper end. The inside and bottom of the tube was covered with a light-reflecting foil. The photon flux density in the chamber was regulated by raising and lowering a metal halogen lamp (Osram HQI TS-400 W) above the chamber. Photon flux density was measured in the chamber by a quantum sensor (LI-190, LI-COR Inc., Lincoln, USA). Air and cone temperatures were measured by copperconstantan thermocouples and the dew point of the air by dew point mirrors (Heinz Walz, Effeitrich, BRD). This gas exchange measurement system has been described in detail by Linder et al. (1980) and Linder and Troeng (1981 a).

Measurement procedure. Cones were detached from the tree together with the shoot from the previous year and immediately placed in a plastic bag and brought into the laboratory where the end of the shoot was recut under water. Needles were removed from the shoot axis and the shoot placed in a test tube with distilled water. The end of the tube was sealed with Parafilm and placed in the chamber in such a way that all sides of the cone were illuminated by direct or reflected light. Large cones had a high thermal inertia; after changing light intensity or air temperature, it took at least 1 h for them to reach a stable temperature. Therefore, measurements on large cones could last for more than 5 h, and to avoid cone desiccation, it proved necessary to suppley water. There were pronounced differences in the pattern of respiration o f the cones with and without water supply (Table 1). With water supply transpiration was more or less constant over a period of 3 days, but without water supply, it rapidly decreased to a low level. The temperature dependence of respiration (Ql0) was determined several times during the season and was found to be 2.0 throughout the entire period. All rates of respiration were normalized to a reference temperature of 20~ using a Qt0 of 2. Respiration in light was measured, while increasing light intensity stepwise up to 900 or 1300 Ixmol m -2 s -~. Cone temperatures at high photon flux densities rose 2 - 3 ~ above air temperature, which was maintained at 20 oC. Dark respiration was measured at the beginning and end of each light response curve. The rate of dark respiration at each light level was estimated by linear extrapolation between the two measurements. Fresh weight of the cones was determined immediately after the measurements of respiration, and dry weight after drying for 48 h at 75 ~ Chlorophyll content in the cone scales was measured according to Linder (1974) with a Chlorophyllometer (AB Lars Ljungberg, Sweden). Air temperatures and photon flux densities in and above the stand were recorded at 10-min intervals in a meterological tower close to the investigated trees. These measurements were part of the basic meterological and ecological measurements at J~idrahs Ecological Research Station (Perttu et al. 1977; Lindroth 1985). Calculations. The field performance of cone net respiration (Rn) was calculated according to Linder and Troeng (1981 a): R, = R20(t) x 2

l0 x

1 - to (t

where Rz0 = dark respiration at 20 ~ t = time; T = air temperature in the stand; to = refixation capacity at light saturation; I = photon flux density; 150 = photon flux density at 50% of maximum refixation.

125 The first part of the equation corresponds to the dark respiration and the second to the carbon dioxide refixation. At high photon flux densities cone temperature is higher than air temperature, resulting in a slight underestimation of R n when using Tin the estimates o f field performance. It was assumed that photon flux densities above the stand were reduced by 20%, to give a reasonable estimate o f the light conditions at the level where most of the cones were found in the canopy (Linder and Troeng 1981a). Daily values of R20 and c0 were found by linear interpolation from Figs. 2 and 4.

Results

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o........

6

o~

t.)

.g_ 4 "E

Purple and green cones differed in their rate of growth and development (Fig. 1). By the end of June, purple cones had achieved 76% of their final weight, compared to 50% for the green cones. The purple cones developed much faster, as indicated by their increase in dry matter content (Fig. 1 b). The size of cones within individual trees varied considerably, in spite of being sampled from branches of the same or the adjacent whorl. The final dry weight in September of green and purple cones was 15.8 g and 11.3 g, respectively. Rates of cone dark respiration at 20~ (Fig. 2) and growth (Fig. 1) were closely related. At the time of budbreak (shoots) the first measured values reached 6.5-7 mg g-l h-m (41-44 lxmol CO 2 kg -~ s-~). During the development of the cones, respiration decreased rapidly and ceased after seed ripening and cone drying at the end of Sep-

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a

i

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75 v

~ 5o 25

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Photon flux

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,

I 1000

I 1500

density (I~E ni2s 1)

Fig. 3. The light response curves o f refixation o f green (solid line) and purple cones (dotted line). The values are given as the percentage of the respiration rate in darkness. The measurements were made on 8 June

o ~

S

Fig. 2. The seasonal course of dark respiration o f green (solid line) and purple cones (dotted line). The measurements were made at 20 ~ in darkness

i 500 i

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...........................

lO

5 40 84 20

b ~

~

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75

0~

. o " ' " " " ' " ~

50

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Fig. 4. The seasonal course of refixation capacity for green (solid line) and purple cones (dotted line). Measurements were made at 20~ and a photon flux density of >900 wE m -2 s -I

9

~)' ..'e'" .e . . . . . . . . . . . I)'" " " "

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!. The dry weight (a) and dry matter content (b) of green and purple cones (dotted line) from May to September. Moving average n = 3 . The curves in a are fitted by hand Fig.

(solid line)

tember (Fig. 2). The respiration rate of purple cones during the initial growth phase was higher than that of green cones, but later in the summer the situation was reversed. The light response curves of CO 2 refixation were similar in both cone polymorphs and resembled a typical light response curve of leaf photo-

126 I

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|

400

~'!N 300

~

20C

~

lOG

M

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$

Fig. 5. The estimated seasonal course of dark respiration (solid line) and net respiration(dotted line)of green cones. The respiration rate is expressed per average cone weight and per day

synthesis (Fig. 3). Light saturation was achieved at 800-900 ~tE m -2 s-', and 50% of maximum refixation at 200 I~E m -2 s -1. Refixation capacity declined during cone maturation (Fig. 4). Green cones had a higher refixation capacity throughout the growing season. Photosynthesis in green cones was able to reduce respiratory losses at the beginning of the growth season by 50%-55%, compared to 40% in purple cones. The extimated daily amounts of dark respiration and CO 2 refixation, when expressed per cone, increased until the end of June, after which there was a steady decline for the rest of the season (Fig. 5). The short-term variations in daily respiration and refixation reflected fluctuations in the daily air temperature and radiation. During the first month of cone development, the daily gain by CO 2 refixation reached 28%-34% in green and 22%-26% in purple cones, but declined during the second month to 15%-20% and 10%- 15%, respectively. Despite the Table 2. The estimated costs of cone production expressed on a single-cone basis. The carbon content was assumed to be 50% of the dry weight (Linder and Troeng 1981a)

Spruce: Cone biomass (g C) Dark respiration (g C) Refixation (g C) Net cost of production (g C) Refixation (%) Net respiration/biomass (%) Pine: a Refixation (%) Net respiration/biomass (%) a

From Linder and Troeng (1981a)

Green

Purple

7.9 5.3 0.9

5.7 4.5 0.7

12.3 17 56

9.5 16 67

31 50

differences in refixation capacity and growth rhythm, the estimated gain over the whole season was similar in the two cone polymorphs, 16%- 17% (Table 2). The chlorophyll content of the cone scales did not show pronounced differences between green and purple cones, ranging from 0.2-0.3 mg Chl g - ' dry matter. No variation in chlorophyll content was found during the growing season, except for a rapid decline during the second half of August. The green cones remained brightly green until mid-August, but differences in cone colour were easily distinguishable until the beginning of September. Only on the side exposed to the sun could some slight discoloration and yellowing of the cone scales be noticed. Discussion

The maximum rate of dark respiration in spruce cones (41-44 Ilmol CO 2 kg-Is-]) during the initial phase of their growth was twice as high as reported for Scots pine cones (Linder and Troeng 1981 a). This corresponds fairly well to the differences in their relative growth rate in June (110 mg g - ' d a y - ' in spruce and 43 mg g - ' d a y - ' in pine), indicating a similarity in their growth respiration coefficients. There was no seasonal maximum in the rate of spruce cone respiration similar to that found in Scots pine (Linder and Troeng 1981a), but instead a steady decline occurred until respiration ceased at the end of September (Fig. 2). This can be explained by the difference in the pattern of development and growth of cones in the two species. The refixation capacity of the cones showed a similar pattern of decrease (Fig. 4). This could be caused by the increase of the ratio between respiring biomasss and photosynthesizing tissue as well as by increasing water stress, expressed as a decrease in relative water content (Fig. 1). Throughout the season the refixation capacity of green cones was somewhat higher than that of purple cones (Fig. 4), but this difference only counterbalanced the differences in growth pattern (Figs. 1 and 2) and did not influence the total carbon economy of the cone polymorphs (Table 2). The refixation capacity was about half that reported for Scots pine (Linder and Troeng 1981 a), which probably is the effect of a lower ratio of photosynthesizing to respiring tissue in spruce cones compared to pine cones. Considering that a cone can be compared to a very thick leaf with pronounced light extinction within the photosynthesizing tissue, it is at first

127 surprising that light saturation occurs at such low photon flux densities, < 9 0 0 liE m-2s -1. The chloroplasts are, however, concentrated to the outer third of the cone scales, and form a thin layer, not exceeding 1 mm, around the cone. This layer is therefore already light-saturated at moderate light levels. In a non-ventilated chamber and at a photon flux density of 1300 liE m-2s -l, the temperature of purple cones rose to 10.7 ~ in green cones 8.5 ~ above the ambient chamber temperature, which was maintained at 20 ~ If the chamber was fully ventilated, the temperature increase was reducted to 3.0 ~ and 2.5 ~ respectively. A similar difference was reported for Abies concolor cones (Sturgeon and Mitton 1980). This indicates that, especially during calm days, there is some risk of underestimating day time respiration in field conditions, when using air temperature instead of actual cone temperature in the calculations. Under a high radiation load the cones, as massive bodies, are unable to dissipate the energy of absorbed short-wave radiation by convection, and their temperature will increase above ambient air temperature. It is possible to calculate cone temperature by using an energy balance approach (Gates 1965), but several additional cone parameters and climatic variables would be needed. In the present study it can only be assumed that the actual amount of cone respiration was not underestimated by more than 5%-10%. Sturgeon and Mitton (1980) listed several hypotheses to explain the advantages of purple cone coloration, but they favoured the thermal theory put forward by Schr6ter (1898). The purple coloration can result in a higher temperature sum (Kozubov 1962), which may be an advantage in extreme climatic conditions. The present results do not contradict this hypothesis, since purple cones developed faster and matured earlier (Fig. 1 a). Refixation of CO 2 reduced carbon costs for cone and seed production by 16%-17%, compared to 30% in Scots pine (Linder and Troeng 1981a). Net respiratory costs for producing cone material were consequently higher for spruce than for pine (Table 2), reflecting the differences in the pattern of cone production. A higher respiratory cost in purple cones can be attributed to their faster growth and development (Fig. 1) and considered as the price for adaptation to a colder climate. The magnitude of the average cost of cone production and its effect on stemwood production in a spruce stand can be estimated using

some simplified assumptions. During an average year in Central Sweden, there are 40 cones per tree (Lindgren et al. 1977). Using the weight of green cones (Table 2) and assuming a stocking of 500 trees ha -I gives an annual cone production equal to 158 kg C ha -l. To this a respiration cost of 88 kg C ha-J should be added giving a total of 248 kg C h a - ' year -l, equal to 496 kg of dry matter. Using a stemwood density of 400 kg m -3 (e. g. Chalupka et al. 1977), 50% carbon content and a respiration coefficient for wood production of 0.67 (Linder and Troeng 1981 b), it can be estimated that 1 m 3 of stemwood requires 334 kg C. On the average, cone production therefore reduces stemwood production in Norway spruce forests in Central Sweden by 0.7 m 3 ha -l year -I. During years with large cone crops, the number of cones per tree may be more than 10 times higher than the average number used here (Lindgren et al. 1977), causing a considerable loss in stemwood production. The high estimates by Rohmeder (1967) may be explained to some extent by converting cone biomass into stemwood biomass without considering the respiratory costs of production, and by the fact that in the southern parts of the distribution area of Norway spruce, cone crops are larger and more frequent (Schmidt-Vogt 1987). The effect on individual trees can be even more pronounced than that at stand level, since dominant trees can carry a heavy crop at the same time as suppressed trees carry no cones at all (Lindgren et al. 1977). Acknowledgements. The authors thank Mr. A. Wikstr6m for his help in processing the data. The senior author wishes to thank The Swedish Institute for the scholarship provided and The Swedish University of Agricultural Sciences for their hospitality.

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128 Danilov VN (1953) Influence of cone production on the structure of the annual growth ring in Norway spruce (Picea excelsa Link.) (In Russian). Bot Zurn 38:367-377 Eis S, Garman H, Ebell LF (1965) Relation between cone production and diameter increment of Douglas fir (Pseudotsuga menziesii (Mirb.) Franco), grand fir (Abies grandis (Dougl.) Lindl.), and Western white pine (Pinus monticola Dougl.). Can J Bot 43:1553-1559 Etverk I (1965) Selection of plus-trees and breeding of Norway spruce (in Estonian) Cand Biol Thesis, Tartu Gates DM (1965) Heat transfer in plants. Sci Am 50:563-573 Kozubov GM (1962) Eine Form von Pinus silvestris mit roten Antheren. (In Russian). Bot Z 47:276-280 Linder S (1974) A proposal for the use of standardized methods for chlorophyll determinations in ecological and ecophysiological investigations. Physiol Plant 32: 154-156 Linder S, Troeng E (1981 a) The seasonal course of respiration and photosynthesis in strobili of Scots pine. For Sci 27: 267-276 Linder S, Troeng E (1981b) The seasonal variation in stem and coarse root respiration of a 20-year-old Scots pine (P/nus sylvestris L.). In: Tranquillini, W (ed) Radial growth in trees. Mitteil Forstl Bundes-Versuchsanst. Wien Ber 142:125-139 Linder S, NordstrSm B, Parsby J, Sundbom E, Troeng E (1980) A gas exchange system for field measurements of photosynthesis and transpiration in a 20-year-old stand of Scots pine. Swed Conif For Proj Tech Rep 23

Lindgren K, Ekberg I, Ericsson G (1977) External factors influencing female flowering in Picea abies (L.) Karst. Stud For Suec 142 Lindroth A (1985) Climate, photosynthesis and litterfall in pine forest on sandy soil - basic ecological measurements at J/idra~s. (in Swedish, English summary). Swed Univ Agr Sci, Dept Ecol Environ Res Rep 19 Perttu K, Lindgren A, Lindroth A, Noren B (1977) Micro- and biometeorological measurements at J~idra~s. Instrumentation and measurements techniques. Swed Conif For Proj Tech Rep 7 Rohmeder E (1967) Beziehungen zwischen Frucht- bzw. Samenerzeugung und Holzerzeugung der Waldb~iume. Mitt Staatsforstverw Bayerns 3 6 : 1 - 2 3 Schmidt-Vogt H (1986) Die Fichte. Ein Handbuch in zwei B/inden. Band II/1. Parey, Hamburg Schmidt-Vogt H (1987) Die Fichte. Ein Handbuch in zwei B~inden. Band I, 2nd ed, Parey, Hamburg Schr6ter C (1898) Ober die Vielgestaltigkeit der Fichte. Viertelj Naturforsch Ges Ziirich 43 : 1- 130 Sturgeon KB, Mitton JB (1980) Cone color polymorphism associated with elevation in white fir, Abies concolor, in southern Colorado. Am J Bot 67: 1040-1045 Teich AH (1975) Growth reduction due to cone crops on precocious white spruce provenances. Bi-monthly Res Notes Can For Serv 31 : 6 Received March 17, 1986