Mar 18, 1994 - mann 1983; Ewers and Zimmermann 1984; Tyree et al. 1987). ..... Shelburne V, Hedden R, Allen R (1993) The effects of site, stand density, and ...
Oecologia (1995) 102:164-168
9 Springer-Verlag 1995
Frank Berninger 9Maurizio Mencuccini 9Eero Nikinmaa John Grace 9Pertti Hari
Evaporative demand determines branchiness of Scots pine
Received: 18 March 1994 / Accepted: 13 December 1994
Abstract Analysis of the branch area/stem area ratio of Scots pine growing in different climatic conditions in Europe and Siberia indicates that the branch area supported by a stem increases in warmer and drier conditions. The ratio was significantly correlated with several climatic variables, especially with potential evapotranspiration (Ep). The ratio was negatively correlated with stand density (ds). A regression model combining Ep and d s accounted for 85% of the total variation. These trends are believed to reflect hydraulic segmentation of trees and may represent a strategy to avoid cavitation in the tree, especially in the branches. Key words Pinus sylvestris 9 Hydraulic architecture 9 Geographic variation- Pipe theory - Branchiness
Introduction Leonardo da Vinci observed that "all the branches of a tree at every stage of its height, when put together, are equal in thickness to the trunk below them" (Richter 1970). Botanists have usually attributed this relationship to the hydraulic demands of a tree, and expressed it as the pipe theory of plant architecture (Shinozaki et al. 1964; Whitehead 1978; Valentine 1985; Hari et al. 1986; M~ikel~i 1986). According to the pipe model, a tree is a simple and ideal transport system: there are no hydraulic F. Berninger ( ~ ) 9E. Nikinmaa 9 R Hari Department of Forest Ecology, PL 24, 00014 University of Helsinki, FIN-00014 Helsinki, Finland FAX +358-0-1917605 M. Mencuccini Institute of Forest Ecology and Silviculture, University of Florence, Via S. Bonaventura 13, 1-50145 Florence, Italy John Grace Institute of Ecology and Resource Management, University of Edinburgh, King's Buildings, Mayfield Road, Edinburgh EH9 3JU, UK
constrictions at nodes and water flow occurs in response to gradients of water tension. Currently, there is some controversy about the applicability of the pipe model, and the hydraulic interpretation. One objection to the hydraulic interpretation of tree architecture is that similar relationships might satisfy also other demands of the tree, such as the need for a mechanically stable structure to support the leaf canopy with the minimal use of structural material. Allometric relationships have often been found between leaf area and stem area, and between branch area and stem area (Whitehead 1978; Hari et al. 1985; A1brektson 1988; Barrantes and Graci 1989; van Hees and Bartelink 1993). Although these relationships are consistent with the pipe model, the observed hydraulic properties of the transport system are not necessarily those of the pipe model: for example leaf-specific conductance changes within the tree (Huber 1928; Zimmermann 1983; Ewers and Zimmermann 1984; Tyree et al. 1987). Here we report the geographical variation in the ratio of branch area to stem area in Scots pine (Pinus sylvestris L.). The tree is widely distributed in Europe and shows great variation in form. Because most of the hydraulic resistance is located in the branches (Ewers and Zimmermann 1984), we might expect that trees in more evaporative conditions would have a higher branch area/stemwood area ratio than trees in less evaporative conditions, because this would reduce cavitation in branches. If, on the other hand, the ratio is set by mechanical constraints we may expect that site windiness and stand density will be correlated with the ratio.
Materials and methods Foliage masses and wood cross-sectional areas were measured in Scots Pine stands in different parts of its natural distribution area (Table 1, Fig. 1). Most stands were the result of natural regeneration, or established by planting with seeds of the same climatic region (sites Siuntio, Hyyti~il~i and Muddusniemi). The stands in Britain were from a German seedlot. A summary of the sites is presented in Table 1.
165 Table 1 Short description of the climatic differencesand structural differences between the stands. (Sources: i Barrantes et al. 1989, 2 Nikinmaa 1992, 3 Berninger et al. (1994), 4 Mencuccini unpublished work; Dbh diameter at breast height; sampling meth-
ods: 1 subjectively from the stand to get the whole sizevariation of trees selected, 2 randomly in two strata, one bigger and one smaller than the median tree)
Site
Coordinates
Meantemperature
Potential evapotranspiration (Thornthwaite method) mm
Dbh (cm)
h (m)
Age (years)
Trees/ha
Sampling method
Source
Muddusniemi Muddusniemi Haapajiirvi Hyytiiilii Siuntio Siuntio Aberfoyle Irkutsk Voronez Thetford Casina La Viale Montesquiu
69 N 27 E 69 N 27 E 62 N 34 E 62 N 24 E 60 N 24 E 60 N 24 E 56N 4 W 53 N 103 E 52 N 40 E 52 N 1 E 44 N 10 E 44 N 4 E 41 N 4 W
-0.5 -0.5 2.6 4.0 4.8 4.8 8.0 -1.2 6.6 9.7 11.4 9.7 12.1
398 398 485 502 510 510 598 464 622 639 698 662 691
3.2 3.7 4.6 11.6 7.34 7.5 13.6 7.2 7.6 21 7.4 6.1 ?
4.3 4.4 3.5 9.4 5 6.1 10.1 6.7 7.5 18.4 8.1 6.9 ?
43 36 28 22 15 17 38 23 16 38 70 22 ?
5300 12000 5830 2900 2000 3500 1432 4900 6320 1146 1814 8000 ?
2 2 1 2 2 2 1 1 1 1 1 2 1
2 3 2 2 3 3 4 2 2 4 4 3 1
month and linear interpolation of the temperatures was used to determine the beginning and end of the growing season. The maximum average monthly evapotranspiration is probably biased due to the shortcomings of the Thornthwaite method (Rosenberg et al. 1983).
Results and discussion
Fig. 1 Location of the sites (A Montesquiu, B Casina, C La Viale, D Thetford, E Voronez, F Irkutsk, G Aberfoyle, H Siuntio, J Hyytiiil~i,K Petroskoi, L Muddusniemi) On the sample trees, the diameter of the branches below the lowest living whorl of subbranches, and the stem diameter below the living crown, were measured. The lowest living whorl of branches and stems was defined so that at least 50% of the main branches of the whorl of branches of sub-branches were still alive. All cross-sectional area in this study are cross-sectional areas below bark. The cross-sectional areas of all branches in each tree were summed. The relationship between the total cross-sectional areas of branches and the stemwood area was always linear. The slope of a regression of branchwood area on stemwood area (6) was calculated using regression analysis without intercept. The intercepts of the regressions were not significant (at the P = 0.01 level) with one exception (Voronez). Climatic data were taken from long-term averages 1930-1960 from the literature (Muller 1982; meteorological service data for Honnington, Aberfoyle and Casina). The nearest weather station in comparable altitude was always chosen. The stations were: Sodankyl~ for Muddusniemi, Helsinki-Ilmala for Siuntio, Tampere for Hyytiiilii, Petrosavodsk for Haapajiirvi, Irkutsk for Irkutsk, Charkov for Voronez, Clermond Ferrand for la Viale, Valladolid for Montesquiu, Casina for Casina, Aberfoyle for Aberfoyle and Honington for Thetford. Potential evapotranspiration estimates were calculated by the Thornthwaite method (Thornthwaite 1948). The length of the growing season was defined as the time where the average temperature is above 5~ It was calculated assuming that the average temperature of the month occurs in the middle of the
The b r a n c h w o o d area to s t e m w o o d area ratio (6) varied b e t w e e n 0.76 and 1.87, and often differed significantly from the value of 1.0 expected from the pipe model. We tried to correlate the structural characteristics of trees with climatic variables and stand properties. 0 was significantly correlated with several climatic variables and with stand characteristics (Table 2, Fig. 2). Table 2 Correlation of 0 with different stand and environmental variables. (Because of the shortcomings of the Thornthwaite method, the maximal potential evapotranpiration might be biased.) The average diameter growth rate is the average tree diameter divided by the stand age Spearman's correlation coefficient
Significance of the correlation, P
Potential evapotranspiration Length of the growing season Average yearly temperature Precipitation Average yearly windspeed Average temperature of the warmest month Maximal monthly potential evapotranspiration
0.93 0.92 0.92 0.32 -0.37 0.61
0.0001 0.0001 0.0001 0.3 0.4 0.03
Average diameter at breast height Height of the trees Number of living whorls Average age of the stand Average diameter growth rate Stand density
0.73 0.78 -0.48 0.11 0.39 -0.60
0.21
0.5 0.008 0.003 0.13 0.04 0.21 0.08
166 Fig. 2 Plot of O against the potential evapotranspiration (mm), average temperature ~ average yearly windspeed (m s-~), average yearly precipitation (ram), stand density (tree ha-l), stand diameter at breast height (cm). (Symbols: A Montesquiu, B Casina, C La Viale, D Thetford, E Voronez, F Irkutsk, G Aberfoyle, H Siuntio 1, I Sinntio 2, J Hyyti~il~i, K Petroskoi, L Muddusniemi 1, M Muddusniemi 2)
1.90-
t.90
A
t.80
C
1JO
A
1.80
C
1.70
1.60
1.60
1.50
D E
1.40 1.30
I
1.20 1.10
1.50
1.1o f 0,90 0,80
L
M
0,70 400.00
500.00
600.00
700.00
nr
3.00
- ~ O0
POTENTIAL EVAPOTRANSPIRATION
1.90
1.80
1.80
1.70
1.70
1.60
1.60
1.50
1.50
1.40
1.40
E
?
1.20
1.1o
C
D E
1.30 1.10
1.00
0.70 2.00
0.80
3,00
4.00
5.00
0.70 30O,O0
WINDSPEED 1,90
1.90 1.80
1.70
1.70
1.60
1.60
800.00
1300.00
C
D
1.40 ]
1.4O
E
1.30
I
1.20
Hj
1,20 1,10 1.00 [
K L
0.90 0.80
7500.00
#
J
o.8o M 0.70.
15000.00
3.00
STAND DENSITY
A problem in the analysis is that the research does not differentiate between sapwood and heartwood area. However previous research indicates (Hari et al. 1985; Kaipiainen and Hari 1986; E..~r61fi, unpublished work), that almost all of the xylem area below the living crown consists of sapwood and it is therefore improbable, that different rates of heartwood formation are responsible for the differences in 0. Also, most of the stands are young and therefore the amount of heartwood is probably small. Another problem with this type of analysis is that the meteorological variables are intercorrelated (Table 3), making it impossible to separate the statistical effects of different variables. In particular, the potential evapotran-
K
0.90- -
M
0.70 0.00
E B I
1.30
B
F
1.00
1800.00
C
1.50
D
1.10
M YEARLY PRECIPITATION
1.80
1.5o
I
L
0.90
M
B
kJ H F
1.00
L
0.80
13.01:
A
1.20
F
0.90
8.00
TEMPERATURE
1.90
1.30
jH
K
1.00
0.80
B
I
1.20
0.90 0,70 300.00
E
1.30
B
FKJ
1.00
D
1.40
8.00
13.00
18.00
23.00
DBH
spiration (Ep), the temperature of the warmest month and the length of the growing season show a strong correlation. There was a less pronounced correlation between stand properties (diameter, stand density and height) and 0. It was postulated that Ep is the most powerful predictive variable. Indeed as much as 79.8% of the variation is accounted for by this variable alone in the regression equation (P = 0.001) where the units of Ep are mm year-1. 0 = -0.281 + 0.00282 Ep
However,we found that the residuals were systematic with respect to stand density d s, and a second regression
167 Table 3 Spearmam's correlation matrix for the climate and stand variables (T=average yearly ternperature, PRE=average yearly precipitation E_=Potential evapotransplratlon, LEN=length of the growing season, W=average yearly windspeed, MT=maximum average monthly temperature ME_= maximum average ' vpotenual 9 evapotransplmonthly ration, H=average height of the trees, LW=averagenumber of living whorls, AGE=average age of the trees, D=stand density.) .
'.
1a
0.3 84
Ep T PRE LEN W MT MEp H LW AGE D
Ep 1 0.97 0.23 0.86 0.51 0.64 0.14 0.55 -0.59 -0.01 -0.40
T 1 0.13 0.86 0.51 0.64 0.14 0.66 -0.42 0.11 -0.44
PRE 1 0.34 -0.05 -0.02 -0.03 0.51 -0.44 0.08 -0.71
0.2.
0.0-0.1
[ C DHJ
/ K E
-0.2 -0.3 -0.4 0.00
W 1 0.19 0.55 0.20 -0.42 -0.55 -0.10
MT l
0.61 0.42 -0.60 0.15 -0.05
MEp 1 -0.02 -0.43 -0.23 0.02
H 1 -0.27 0.14 -0.62
LW 1 0.90 0.04
AGE 1 -0.28
D 1
es in 0, might therefore either increase the water tension in branches but simultaneously decrease the risk of cavitation at more negative pressures, or decrease the tension in structures that have wider vessels and are cavitated more easily. The interrelationship between flows, water tensions, permeabilities and water conducting areas of interconnected hydraulic conductors may be investigated using Darcy's law. Assuming no change in water storage, the flow rate along the stem and the sum of the branches must be the same. So at each whorl we have:
0
0.1.
LEN 1 0.21 0.74 0.33 0.67 -0.38 0.19 -0.44
ksAsAWs _ kbAbAWb _ kbAsAWb 5000.00
10000.00
15000.00
S T A N D DENSITY
Fig. 3 Residual plot of the first regression model (0 as independent variable) against stand density (trees ha-1) Symbols as in Fig. 2 equation accounted for 85.0% of the residual variation (Fig. 3): 0 = 0.217 + 0.00213 E p - 0.0000315 d s where the unit of d s are trees ha -1. Both regressors are significant at the 5% level. Regressions of other climatic variables together with stand density gave similar results, but other stand variables were not significant in combination with climatic variables. The correlation of 0 with stand density can be explained in two ways: either it is a response to higher mechanical stimulation (Jacobs 1939, 1954; Larson 1963; Valinger 1992) an acclimation to a lowered hydraulic conductivity due to smaller tracheid sizes in suppressed trees (Shelburne et al 1993; Sellin 1993). However 0 was not correlated with the diameter growth rate of the stand. Therefore, it is improbable that changes in 0 are ascribable to the differences in relative growth rate and associated changes in tracheid diameter. The boundary layer resistance is probably lower for open stands, but this should have only a minor influence on transpiration, because coniferous canopies are usually closely coupled to the atmosphere (Rosenberg 1983). Carlquist (1988) hypothesized that wood structures with a higher hydraulic permeability would be more prone to cavitation, whereas wood structures resistant to cavitation would have a low permeability. Changes in the wood structure, occurring parallel to the observed chang-
where the subscripts indicate stem (s) and branch (b) properties, k is the sapwood permeability, A s is the crosssectional area of the stem, A b is sum of the cross-sectional area of the branches, g is the viscosity of the water, A W is the water tension drop, l is the length of the stem or branch segment and 0 is the branch area:stem area ratio. If we assume that 1 and g do not change between the different locations the following should be true:
~ _ A9 = ksaWs Thus changes in 0 lead to changes in the water tension gradients of stern and branches, if the ratio of stem and branch sapwood permeability does not change. An increase in 0 implies that the pressure gradient in branches is lower than in stems. In practice, this is expected to reduce the probability of cavitation. In a hot dry climate, or a climate with frequent droughts, this character would give selective advantage provided that it did not mean that cavitation occurred in the stem instead. There is evidence that the anatomy of the xylem varies with latitude and climate, becoming more resistant to cavitation at dry sites. In angiosperms lumen area and tracheid length both decrease with latitude, indicating that the xylem conductivity is higher where the potential evapotranspiration is higher (van den Oever et al. 1981; Baas et al. 1983; Baas 1986; Zhang et al. 1992). In Scots pine a similar trend for tracheid length is indicated from the studies of Schulze-Dewitz (1968) and Echols (1958) (different provenances at one location). The small tracheid sizes in the northern locations might be an acclimation to avoid freezing embolism (Ewers 1985). Because freezing embolism affects all aboveground parts of a tree
168 a s m a l l e r 0 c o u l d b e e x p e c t e d for c o l d places, but on the other h a n d w a r m c o n t i n e n t a l p l a c e s like Voronez have s i m i l a r w i n t e r c o n d i t i o n s to m o r e northern, m o r e m a r i t i m e p l a c e s such as M u d d u s n i e m i . A l l these lines o f evidence, and the strong correlation o f 0 and Ep, point to the likely i m p o r t a n c e o f the evaporative d e m a n d and h y d r a u l i c aspects o f tree architecture as the p r i m e d e t e r m i n a n t o f the tree architecture. T h e data do not support the h y p o t h e s i s that 0 is d e t e r m i n e d p r i m a r ily b y m e c h a n i c a l loading. T h e r e is no relationship bet w e e n 0 and the m e a n w i n d s p e e d o f the site, and the relationship b e t w e e n 0 and the stand density (which m i g h t inf l u e n c e the m e c h a n i c a l stimulation r e c e i v e d b y trees) is w e a k e r than the climatic d e p e n d e n c i e s . A v o i d a n c e o f cavitation m i g h t b e the cause o f these changes in structure, but further research on the h y d r a u l i c p r o p e r t i e s and the r e g u l a t i o n o f transpiration is n e c e s s a r y to further c o r r o b o rate this hypothesis. A better u n d e r s t a n d i n g o f the a d a p tive significance o f b r a n c h i n e s s m i g h t i m p r o v e our understanding o f growth and strucutural d e v e l o p m e n t o f trees and stands and helps to p e r c e i v e limitations to the imp r o v e m e n t o f quality o f conifers through breeding. Acknowledgements We thank the European Science foundation, the Consiglio Nazionale delle Ricerche (Italy) and the Finnish Academy for financial support. Part of the research was also supported from the British Council M.U.R.S.T. agreement (project: Ecological significance of cavitation in woody plants). We are also indepted to Professor Carlos Gracia (C.R.E.A.F. Barcelona), Professor P. Piussi (University of Florence), Dr. Maurice Rapp (Centre 6cologique Luis Emherger) and to Luca Cocchi, Gipo Gandolfo, Pekka Kuitunen and J6rn Laxen.
References Albrektson A (1988) Sapwood basal area and needle mass of Sots pine (Pinus sylvestris L.) trees in central Sweden. Forestry 57: 3543 Baas P (1986) Ecological patterns in xylem anatomy. In: Givinish TJ (ed) On the economy of plant form and function. Cambridge University Press, Cambridge, pp 327-349 Baas P, Werker E, Fahn A (1983) Some ecological trends in vessel characters. IAWA Bull 4:2-3:141-159 Barrantes O, Gracia CA (1989) Estimation del area foliar a partir de la superficie de albura en Pinus sylvestris. Options Mdditerrantens- Sdric stminaires 3:53-56 B erninger F, Nikinmaa E (1994) Within tree and between site variation in the foliage area-sapwood area relationships in Scots pine stands in different climatic condictions. Can. J. For. Res. 24:2263-2268 Carlquist S (1988) Comparative wood anatomy: systematic, ecological and evolutionary aspects of dicotyledon wood. Springer, Berlin Heidelberg New York Echols RH (1958) Variation in tracheid length and wood density in geographic races of Scots pine (Bulletin 64). School of Forestry, Yale University, New Haven Ewers FW (1985) Xylem structure and water conductivity in conifer trees, dicot trees and lianas. International Association of Wood Anatomists Bull 6:309-317 Ewers FW, Zimmermann MH (1984) The hydraulic architecture of balsam fir (Abies balsamea). Physiol Plant 60:453-458
Hari P, Kaipiainen L, Korpilahti E, M~ikeRi A, Nilsson T, OkerBlom P, Ross J, Salminen R (1985) Structure, radiation and photosynthetic production in coniferous stands. Univ Helsinki Dep Silvicult Res Notes 54:1-233 Hari P, Heikinheimo P, MS_kel~iA, Kaipiainen L, Korpilahti E, Salmela E (1986) Trees as a water transport system. Silva Fenn 20:205-210 Hees AFM van, Bartelink H (1993) Needle area relationships in Scots pine in the Netherlands. For Ecol Manage 58:19-31 Huber B (1928) Weitere quantitative Untersuchungen fiber das Wasserleitungssystem der Pflanzen. Jahrb Wissensch Bot. 67: 877-959 Jacobs MR (1939) A study of the effect of wind sway on trees (Bulletin 26). Australian Commonwealth Forestry Bureau, Canberra Jacobs MR (1954) The effect of wind sway on the form and development of Pinus radiata D. Don. Aust J Bot 2:35-51 Kaipiainen L, Hari P (1985) Cosistencies in the structure in Scots pine. In: Tigerstedt PMA, Puttonen P, Koski V (eds) Crop physiology of forest trees. Helsinki University Press, Helsinki, pp 32-37 Larson PR (1963) Stem form development of forest trees. For Sci Monogr 5:1-41 Mfikel~i A (1986) Implications of the pipe model theory on dry matter partitioning and height growth of trees. J Theor Biol 123:103-120 Mfiller MJ (1982) Selected climatic data for a global set of standard stations for vegetation science. Junk, The Hague Nikinmaa E (1992) Analysis of the growth of Scots pine: matching the structure with the function. Acta For Fenn 235:1-68 Oever L van den, Baas P, Zandee M (1981) Comparative wood anatomy of Symplocos and latitude and altitude of provenance. IAWA Bull 2:3-24 Richter JP (1970) The notebooks of Leonardo da Vinci (1452-1592), compiled and edited from the original manuscripts. Dover, New York Rosenberg NJ, Blad BL, Verma SB (1983) Microclimate: the biological environment. Wiley, New York Schulze-Dewitz G (1968) Einfluss der Vegetationszeit auf einige Strukturmerkmale bei Kiefernholz. Holzindustrie 21:55-58 Sellin A (1993) Resistance to water flow in xylem of Picea abies (L.) Karst. trees growing under contrasting light conditions. Trees 7:220-226 Shelburne V, Hedden R, Allen R (1993) The effects of site, stand density, and sapwod permeability on the relationship between leaf area and sapwood area in loblolly pine (Pinus taeda). For Ecol Manage 58:193-209 Shinozaki K, Yoda K, Hozumi, Kira T (1964) A quantitative analysis of plant form - the pipe model theory. I. Basic analyses. Jpn J Ecol 14:97-105 Thornthwaite CW (1948) An approach toward a rational classification of climate. Geogr Rev 38:55-94 Tyree MT, Flanagan LB, Adamson N (1987) Response of trees to drought. In: Hutchinson TC, Meema KM (eds) Effects of atmospheric pollutants on forests, wetlands and agricultural ecosystems (NATO ASI series vol G16). Springer, Berlin Heidelberg New York, pp 201-216 Valinger E (1992) Effects of wind sway in stem form and crown development of Scots pine (Pinus sylvestris L.). Aust For 55: 15-21 Valentine HT (1985) Tree-growth models: derivations employing the pipe model theory. J Theor Biol 117:579-584 Whitehead D (1978) The estimation of foliage area in Scots pine. Forestry 51:137-149 Zhang SY, Baas P, Zandee M (1992) Wood structure of the Rosaceae in relation to ecology, habitat and phenology. International Association of Wood Anatomists Bull 13:307-349 Zimmermann MH (1983) Xylem structure and the ascent of sap. Springer, Berlin Heidelberg New York
