Climatic factors controlling reproduction and growth of Norway spruce ...

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Climatic factors controlling reproduction and growth of Norway spruce in southern Norway Vidar Selås, Gianluca Piovesan, Jonathan M. Adams, and Mauro Bernabei

Abstract: Time series of seed production and tree-ring width of Norway spruce (Picea abies (L.) Karst.) in southern Norway were analysed for their relationship to various climatic factors occurring during “key” stages, which a priori might be expected to show a strong climate response. The following factors combined in a multiple linear regression model were found to predict seed production (based on withheld data points) with considerable accuracy, at high levels of statistical significance: June–July mean temperature and August lowest temperature in the previous year, late spring frost and June–July precipitation of the last 2 years, and January–February lowest temperature in the current year. Tree ring width was negatively correlated with the seed production index of the current year and the lowest July temperature in the previous year and positively correlated with June–July precipitation in the current year. It is suggested that habitat constraints for seedling establishment should also be considered in a more general life-history cost theory to explain masting behaviour in forest trees. Résumé : Des séries temporelles de données de production de graines et des largeurs de cerne annuel d’épicéa commun (Picea abies (L.) Karst.) du sud de la Norvège ont été analysées pour déterminer quelle était leur relation avec différents facteurs climatiques lors de stades clés, qui devraient a priori réagir fortement au climat. Les facteurs suivants combinés dans une équation de régression linéaire multiple peuvent prédire la production de graines (sur la base de données non utilisées) avec une très grande précision et de façon statistiquement très significative. Ces facteurs sont la température moyenne des mois de juin et juillet et la plus basse température du mois d’août de l’année précédente, le gel tardif au printemps et les précipitations des mois de juin et juillet des deux dernières années ainsi que la plus basse température des mois de janvier et février de l’année courante. Il y a lieu de croire que les contraintes liées à l’habitat pour l’établissement des semis devraient également être prises en considération dans une théorie plus générale du coût du cycle biologique pour expliquer le comportement des arbres forestiers en lien avec la production de semences. [Traduit par la Rédaction]

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Introduction Masting behaviour in forest trees has long been a theme of research and discussion (e.g., Kelly 1994; Herrera et al. 1998; Kelly et al. 2001). Although its broad phenomenology is well described in most cases, the physiology of masting presents many aspects worth investigating. Mast years are not consecutive because of an endogenous cycle, which in fruit trees is known as alternate bearing (Crawley and Long 1995; Kozlowski and Pallardy 1997). Several studies have shown that particular climatic conditions during the time of floral induction enhance flower production and that weather also has important effects on flower and fruit development (e.g., Holmsgaard 1962; Wachter 1964; Sork et al. 1993; Owens 1995). Received 9 April 2001. Accepted 11 October 2001. Published on the NRC Research Press Web site at http://cjfr.nrc.ca on 23 January 2002. V. Selås.1 Department of Biology and Nature Conservation, Agricultural University of Norway, P.O. Box 5014, N-1432 Ås, Norway. G. Piovesan and M. Bernabei. Department of Forest Science, University of Tuscia, Via SC de Lellis, I-01100 Viterbo, Italy. J.M. Adams. Department of Natural Resources Science, University of Rhode Island, RI 02879, U.S.A. 1

Corresponding author (e-mail: [email protected]).

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Few studies have analysed how climate variations simultaneously control growth and reproduction of a species on a regional scale (Holmsgaard 1962; Woodward et al. 1994; Piovesan and Bernabei 1997). While a great deal of research has dealt with tree-ring climate relationships (e.g., Fritts 1976; Cook and Kairiukstis 1990), several aspects of the influence of climate on reproductive behaviour of trees remains unknown, especially on a decadal time scale. This is a fundamental aspect of plant biology, not only of interest for its own sake, but also because it can leave its mark in the woody growth of the tree, complicating tree-ring climate studies and the proxy reconstruction of climate variations. There is an ongoing debate on climate change and its effects on plants, but to date little is known about how trees in different biomes and ecoregions respond to the magnitude and pattern of climatic variations, especially in terms of reproduction. In this paper we use a dendroclimatological approach to study how much reproduction and also growth (in terms of tree-ring width) of Norway spruce (Picea abies (L.) Karst.) in southern Norway are influenced by climatic variations. During the year a spruce tree passes through certain critical stages (e.g., dehardening, bud burst, flowering, shoot elongation, flower induction, hardening), during which climate may exert a strong control on its behaviour (e.g., Tirén 1935; Eklund 1954; Lindgren et al. 1977; Pukkala 1987; Repo 1992; Lundmark et al. 1998; Hannerz 1999). Combined tree-ring and seed cone chronology, being the result of

DOI: 10.1139/X01-192

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the integration of both vegetative and reproductive processes, permits further investigation of how the whole plant responds to climatic variations. Clarifying these aspects will probably aid understanding of the physiological mechanisms for climatic control of Picea’s geographical range with special reference to its distribution in the west (Bradshaw et al. 2000). Finally, this study may shed some light on the various different hypotheses of the evolutionary ecology of masting behaviour.

Material and methods Study area The study area covers 2971 km2 in the eastern part of Aust-Agder County in southern Norway, and includes the municipalities of Vegårshei, Tvedestrand, Åmli, Froland, Arendal, Risør, and Gjerstad (Fig. 1). The study area is situated in the boreo-nemoral zone, the climate is suboceanic, and snow usually covers the ground from December through March or April. The study area is dominated by forests, mostly of poor and intermediate productivity, with scattered lakes, bogs, and less than 2% agricultural land. Forests with timber production high enough for commercial utilization cover approximately 55% of the total area. At present the forests are characterized by a fine-grained mosaic of young, medium, and old-aged coniferous, mixed, and deciduous stands. Scots pine (Pinus sylvestris L.), Norway spruce, sessile oak (Quercus petraea Liebl.), aspen (Populus tremula L.), and birch (Betula spp.) are the dominant tree species. Seed series As an index of the annual seed production of spruce for the period 1971–1999, we used the mean values of the subjective estimates of cone crops reported by local forest authorities to the National Works of Forest Seed. The study area is divided into five management areas. In each of these five areas, the frequency of trees with seed production was estimated by the forest authorities each year (value 0–1). In addition, they categorized the number of cones on trees with seed production as poor (value 0.3), good (0.5), very good (0.7), or excellent (1.0). For the entire study area, we used the annual mean value for the frequency of trees with seed production, and the annual mean value for the number of cones on seed-producing trees. Then, an annual spruce seed index was calculated by multiplying the index for trees with seeds with the index for cone number on trees with seeds. Tree-ring series Increment cores were extracted at breast height level from 40 spruce trees that were older than 40 years in 1970, which corresponds to the average age at which spruce trees start to reproduce. The trees were sampled from 32 sprucedominated forest stands, representing the different regions of the seed series study area. Within each stand, one or two dominant spruce trees were selected. Trees growing near watercourses, lakes, or bogs were avoided. All increment cores were polished by hand, visually cross-dated, and ring widths were measured to the nearest 0.01 mm using a binocular microscope and a sliding stage

Can. J. For. Res. Vol. 32, 2002 Fig. 1. Map of Norway showing the location of Aust-Agder County (solid area), and map of Aust-Agder showing the seven municipalities (solid area) selected as the study area. The size of the study area is 2971 km2. Data on precipitation were obtained from two meteorological stations (M) within the study area, while data on temperatures were obtained from the station located west of the study area.

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micrometer interfaced with a personal computer (Aniol 1987). The individual series were checked for errors using computer-aided techniques. The site chronology was constructed averaging all the 40 tree-ring series. Climatic series Data on weather was provided by the Norwegian Meteorological Institute. The data series on precipitation were the mean values obtained from two meteorological stations (Nelaug and Vegårshei) situated within the study area (Fig. 1). Data series on temperature were taken from a meteorological station (Byglandsfjord) located outside the study area (Fig. 1), because of missing values from the one that measured temperatures within the study area. For the period 1971–1999, there was, however, a highly significant correlation (P < 0.0001) between the two meteorological stations with regard to the annual fluctuation in the mean temperature in each of the months used in the present study (January: r = 0.99; February: r = 0.99; April: r = 0.97; May: r = 0.97; June: r = 0.98; July: r = 0.97; August: r = 0.98). © 2002 NRC Canada



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Fig. 2. Schematic illustration of climatic and endogneous factors expected to influence positively on the seed production of Norway spruce.

Flower induction

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Data analysis We used multiple-regression models to test for relationships between the seed production or tree-ring series and weather variables. In previous studies, early summer temperatures 1 and 2 years earlier appeared to be important for the seed production of spruce (Brøndo 1972; Pukkala 1987; Luomajoki 1993). Therefore, we first tested for relationships between the spruce seed index and the mean temperature in June–July 1 and 2 years prior to the seed production. Especially during the flower induction period in June–July prior to the flowering year, weather conditions should be expected to show a strong influence on the level of flowering and seed production (Pukkala 1987; Fig. 2). Other recognized critical periods for seed production of spruce are (i) the winter prior to seed production, when low temperatures may damage flower buds; (ii) the period of beginning meiosis in spring (both in the flower induction and flowering year), when late frost events may damage buds or the flower development; and (iii) the period of pollination and fertilization in June–July (e.g., Jonsson 1974; Luomajoki 1993; Owens 1995; Leadem et al. 1997; Fig. 2). However, temperatures during frost hardening in July–August also may be of importance. Generally, the development of frost hardiness starts with growth cessation that is induced both by short days and low temperatures (e.g., Repo 1992; Westin et al. 1995). As a result of cool nights during July– August, trees may start hardening by accumulating reserves in the wood (starch and sugars; Aronsson et al. 1976; Ögren et al. 1997). In this way they are prepared for early frost in autumn, which is common in this region, and in the next growing season they can utilize the accumulated starch for vegetative growth and (or) reproduction. We used two variables to reflect weather conditions during frost hardiness: the lowest temperature in July and the lowest temperature in August. Precipitation in June–July was expected to influence negatively both flower bud induction and pollination and fertilization (Lindgren et al. 1977). To limit the number of predictor variables, we used an index based on the average monthly amount of precipitation during June–July of both the flower-induction and flowering year. As an index of winter cold stress we used the mean of the lowest daily temperature measured in January and February. Late frost events in spring were expressed as the mean value of all daily minimum temperatures below –2°C from 15 April onwards (average date of beginning of meiosis in southern Scandinavia; Luomajoki 1995). The value was set to zero if there were no

days with temperatures below this value during 15 April – 15 May. Late frost in spring may be detrimental both for floral induction and flowering. Hence, as for the June–July precipitation index, the spring frost index used was the mean of the last 2 years. The seed-production index was used as independent variable when analysing for effects of climate on the tree-ring growth, because reproduction was expected to have an inhibitory effect on the vegetative growth (e.g., Holmsgaard 1962; Schweingruber 1996). Different tree-ring studies have shown that wood growth in spruce may be particularly sensitive to summer weather (e.g., Desplanque et al. 1998; Mäkinen et al. 2000). In addition to rain and temperature in June–July of the current and previous year, we also used the lowest temperature in July and in August as independent variables. Statistical analyses were performed using SYSTAT version 7.01. None of the explanatory variables used were significantly correlated. The residuals from the regression models did not differ from a normal distribution, and neither did they show any significant autocorrelations.

Results Seed-production series The coefficient of variation of the spruce seed-production series was 1.2, indicating a variable seed output, typical of a normal masting species (Kelly 1994; Kelly et al. 2000). The seed-production series showed a positive correlation with the mean temperature in June–July in the preceding year (r = 0.63, P < 0.001), while a negative correlation was found with the June–July temperature 2 years earlier (r = −0.70, P < 0.001). Despite a negative lag-one autocorrelation in the June–July temperature index (r = –0.56, P = 0.002), both effects remained significant in a multiple-regression model (1 year earlier: standard coefficient = 0.34, P = 0.035; 2 years earlier: standard coefficient = –0.51, P = 0.003). This model explained 57% of the variance in the seedproduction index (Fig. 3A). The result confirms that summer temperatures 1 and 2 years before seed production can be used to explain some of the seed production variations in Norway spruce, at least in Scandinavia (Brøndo 1972; Pukkala 1987; Luomajoki 1993). However, there were important differences between the predicted and observed seed series, especially in correspondence of high seed-production years (Fig. 3A). The same problem is present in the model of Pukkala (1987). © 2002 NRC Canada



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Fig. 3. Observed seed-production index of Norway spruce in Southern Norway (solid line) compared with the seed index predicted from a linear multiple-regression model (broken line). (A) Untransformed seed-production index in relation to the mean temperature in June– July 1 and 2 years prior to the seed production. (B) Seed-production index where the first-order autocorrelation structure was removed using an ar1 model. The independent variables were the same as in Table 1. 0.6

Spruce seed index

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Table 1. Results from a multiple-regression model with the seedproduction index of Norway spruce in southern Norway as response variable and weather indices as explanatory variables (R2 = 0.80, P < 0.001). Explanatory variable Mean temperature June–July preceding year Lowest temperature August preceding year Mean late spring frost temperature last 2 years Mean June–July precipitation last 2 years Mean minimum temperature January– February

Standard coefficient

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0.4). 50

Spruce tree ring index

resulting in a reduction of the photosynthesis (Lundmark et al. 1998). Much rain in early summer, both in the flower induction and flowering year, appeared to have a negative effect on seed production. The reason is probably that in the year prior to the seed production, a drought during early summer stimulates floral induction, while in the seed production year, dry weather favours the pollen dispersion by wind and then positively influences the fertilization of female cones. Although rain may assist the pollination drop in the pollenscavenging process of several conifers including spruce (Owens et al. 1998), periods with heavy rain, which are common in southern Norway, may interfere with pollination and fertilization (Leadem et al. 1997; Greene et al. 1999). Seed production had a pronounced negative effect on the tree-ring growth of Norway spruce, confirming what has long been known in dendrochronology, i.e., that developing cones are a major sink for assimilates (Schweingruber 1996). The drop in the ring width during a mast year can be as much as 50% compared with a year with the same ecological–climatic characteristics but no seed production (Holmsgaard 1962; Piovesan and Bernabei 1997). During mast years, competition for nutrients may lead to the abortion of pollinated ovules and abscission of conelets in pine (Owens 1991b), which is another endogenous mechanism to preserve the tree’s potential for future reproductive efforts. When a mast year is coincident with an early summer drought, most trees show a very narrow ring width characterized by a growth reduction with respect to the prior year. In tree-ring site chronology, negative pointer years appear as profound minima. In this study, all pointer years were coincident with mast years. This is an important result, because it permits the reconstruction of a sample of mast years from tree-ring series. However, some authors suggest that when the amount of resources available (e.g., water, temperature, light) is not limiting, the seed production may not represent a cost for the tree (see Mencuccini and Piussi (1995) for the specific case on Norway spruce). In fact, the supertree “can only be super under particular environmental condition” (Reznick et al. 2000). Hence, the assumption of costs of reproduction remains an important aspect of life-history evolution, especially in explaining masting behaviour. In contrast to seed production, the vegetative growth seemed to be stimulated by rainy weather during early summer. Spruce is particularly in need of water during the growing season, perhaps because of its superficial root system and high transpiration rates (Desplanque et al. 1998). In spruce, symptoms of crown transparency are often associated with a lack of water (Webster et al. 1996), also in southeastern Norway (Strand 1997). In southern Norway, tree-ring growth appeared to be insensitive to summer temperature of the current year, at least since 1971. This is in agreement with other studies from Scandinavia, where effects of precipitation on tree growth have been found only in the southern region. When moving northwards, summer temperature became the leading limiting factor (see Mäkinen et al. 2000). Norway spruce has the same behaviour on the Alpine cenocline, where from the lower altitudes to the subalpine belt it changes its weather requirements for good woody growth from a wet summer to a warm summer (Desplanque et al. 1998). Further dendroclimatological stud-

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ies are needed to investigate if such climatological behaviour of spruce in southern Norway can be linked to reduced sensitivity to summer temperature of high-latitude tree growth in recent decades (Briffa et al. 1998; Barber et al. 2000). If we omitted the seed index as independent variable in the tree-ring analysis, the three climatic factors June–July precipitation, lowest July temperature in the previous year, and mean June–July temperature in the previous year explained 66% of the variance. As in the case of tree-ring growth in beech (Fagus sylvatica L.) (Piovesan and Schirone 2000), tree rings were wider if the summer weather in the preceding year (cool for Norway spruce and wet for Italian beech) depressed flower induction. The behaviour was, thus, the opposite of that of reproduction. It is now clear that such contrasting responses to the same climatic factor are due to the reproductive aspect of plant life (masting behaviour), which also affects the vegetative growth. Hence, the negative response to summer temperature in the year preceding treering growth found in Norway spruce in Finland (Mäkinen et al. 2000) can probably be linked to the reproductive cycle. In this paper we have demonstrated that masting behaviour can be explained in terms of an endogenous plant cycle and responses to external factors, mainly climate variations. Regarding climatic factors, the central role of a warm dry summer as well as a cool August the year before seed production can be linked to the old idea of stress-induced flower primordium initiation (see Forcella 1981). However, there may also be evolutionary advantages by using a warm dry summer as a cue for the production of a high seed crop. Severe drought can lead to large-scale mortality of trees (Innes 1992). Besides, hot dry weather during summer facilitates forest fires, which often destroy trees over large areas in the boreal region (Larsen and MacDonald 1995; USDA Forest Service 2001). This is the optimum time for seedling establishment because of weakened competition of higher strata in the forest. In some species, fire itself can be a cue for a massive flower-induction phenomenon. It is well demonstrated that fire is the trigger for high seed production in different species, especially in monocots (e.g., palmettos, © 2002 NRC Canada



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bamboos) adapted to fire-prone environments (Abrahamson 1999; Keeley and Bond 1999). There are different selective disadvantages associated with masting behaviour both for parent trees (Waller 1993; Selås 2000) and seedlings (Hett 1971; Sato 2000). Masting behaviour may be explained by different nonmutually exclusive hypotheses, between which predator satiation and wind pollination are up to now believed to have a prior role (e.g., Herrera et al. 1998; Kelly et al. 2001). However, habitat constraints for seedling establishment should also be considered (Sork 1993; Wright et al. 1999) in a more general lifehistory costs theory (Waller 1993; Kelly 1994) to explain masting behaviour in forest trees. We believe that the high seed output in Norway spruce after a warm dry summer is not only a cue trees use to synchronize their reproductive cycle but also an adaptive response to changing environments in the forest.

Acknowledgements We are grateful to I. Fystro at the National Works of Forest Seed and J.A. Kroken, L. Løhaugen and R. Næss at the County Governor’s Office in Aust-Agder, for providing annual reports on spruce seed production.

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