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Norway spruce cone crops in uneven-aged stands in southern Finland: A case study
Forest Ecology and Management 390 (2017) 68–72
Contents lists available at ScienceDirect
Forest Ecology and Management journal homepage: www.elsevier.com/locate/foreco
Norway spruce cone crops in uneven-aged stands in southern Finland: A case study Markku Nygren a,⇑, Kaisa Rissanen b, Kalle Eerikäinen c, Timo Saksa a, Sauli Valkonen d a
Natural Resources Institute Finland, Suonenjoki Unit, Juntintie 154, FI-77600 Suonenjoki, Finland Department of Forest Sciences, University of Helsinki, P.O. Box 27, FI-00014, Finland c Suomen Sijoitusmetsät Oy, Länsikatu 15, FI-80110 Joensuu, Finland d Natural Resources Institute Finland, Latokartanonkaari 9, FI-00790 Helsinki, Finland b
a r t i c l e
i n f o
Article history: Received 15 December 2016 Received in revised form 13 January 2017 Accepted 16 January 2017
Keywords: Picea abies (L.) Seeds Flowering Regeneration Uneven-aged management Image analysis
a b s t r a c t Norway spruce cone crops in individual trees from two seed ripening years 2012 and 2014 were studied. Data were collected from five stands in southern Finland, managed by single-tree selection harvests since the 1980s. The upper third of living crown of each individual tree was photographed for digital cone counting with image analysis. The average number of cones per tree for trees bearing any cones was 92 in 2014 and 66 in 2012. Highest cone numbers found per individual tree were 526 in the year 2014 and 364 in the year 2012. Of all trees studied, 55.5% produced cones during both years, 9.6% produced cones once and 34.9% did not produce cones in 2012 or 2014. The number of cones per tree in 2014 was positively correlated with tree diameter at breast height and the presence of cones (at least twenty) in that particular individual two years earlier and negatively correlated with local basal area. The quality of the seed crop in 2014 as determined in two of the stands was poor. Based on X-ray analyses, 44% of seeds were empty, 29% were damaged by insects feeding on seeds (Plemeliella abietina or Megastigmus strobilobius) and only 25% were full and capable of germination. The results have implications for management practices in uneven-aged Norway spruce stands. It is suggested that at each harvest entry, some large, prolific trees should be retained in order to increase the total number of seeds produced in a stand to enhance regeneration and the recruitment of new seedlings. Ó 2017 Elsevier B.V. All rights reserved.
1. Introduction Norway spruce in Fennoscandia shows high year-to-year variation in cone and seed production. In southern Finland, for example, abundant cone crops generally occur only once or twice a decade. In northern Finland, good cone crops are even less frequent (Tiren, 1935; Sarvas, 1957; Koski and Tallqvist, 1978; Pukkala et al., 2010) and seed maturation in this region may be incomplete due to harsh climatic conditions (Opsahl, 1952; Almqvist et al., 1998). Furthermore, Norway spruce seed crops are often of poor quality, as seeds are frequently destroyed by insects (Hokkanen, 2000). Also, in poor flowering years, the number of empty Norway spruce seeds is high, ranging from 50 to 90% (Andersson, 1965; Sarvas, 1968). Historically, Norway spruce cone and seed crops have been intensively studied in all Nordic countries, though older informa-
⇑ Corresponding author. E-mail addresses: [email protected] (M. Nygren), [email protected] (K. Rissanen), [email protected] (K. Eerikäinen), [email protected] (T. Saksa), [email protected] (S. Valkonen). http://dx.doi.org/10.1016/j.foreco.2017.01.016 0378-1127/Ó 2017 Elsevier B.V. All rights reserved.
tion is based on data from trees growing in even-aged stands. The results of these studies may not be directly applicable to selection stands because of different stem counts, basal area and stand structure in uneven-aged stands (Valkonen and Maguire, 2005). Norway spruce cone and seed crops are also characterized by large variations between individual trees in a stand. The percentage trees that flower varies, depending on whether it is an abundant or scarce flowering year. Koski and Tallqvist (1978) found that in abundant flowering years, the percentage of nonflowering trees is between 2 and 10%, whereas during the years of scarce flowering, this percentage is 55–98%. Thus, only a small part of the trees may produce the bulk of cone and seed crops, particularly in poor seed years. During a 12-year monitoring period, in an 80year-old, even-aged Norway spruce stand in southern Finland, 20% of individuals produced 50% of the total cone crop (Annila, 1981). Generally, dominant and codominant trees produce heavier and more frequent cone crops than intermediate trees; the latter, in turn, produce heavier and more frequent crops than suppressed trees (Heikinheimo, 1932; Waldron, 1965). Moreover, both cone
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size and the number of seeds in an individual cone are positively correlated with tree size (Heikinheimo, 1932; Andersson, 1965). The high year-to-year variation in cone and seed production of Norway spruce presents a challenge to all types of natural regeneration of spruce stands. Synchronous production of large seed crops followed by small seed crops, ie. masting (Silvertown, 1980) has special implications on selection stands with generally continuous seed production as well as the establishment of new seedlings are required for sustainable management. The objective of this case study was to examine the quantity and quality of cone and seed crop in individual Norway spruce trees in stands managed with single-tree selection.
2. Material and methods The data for this study was collected from permanent sample plots established by the Finnish Forest Research Institute (nowadays Natural Resources Institute Finland), in five stands dominated by Norway spruce in southern Finland and managed by single-tree selection harvests since the 1980s. The stands represent samples of either distinct selection structures due to past selection treatments or different stages of transition from an irregular structure towards some, yet unknown, sustainable selection structure (Saksa and Valkonen, 2011). The area of each stand was about 2 ha. They were grown on mineral soils, and the forest site type was either mesic OxalisMyrtillus or submesic Myrtillus type. Specifically, we used the multiple density plots (cf. Eerikäinen et al., 2007) established in these stands from 1992–1994. These plots are rectangular (80 m 100 m) areas, each divided into 8 subplots (20 20 m) with 10-m buffer zones. Subplots form a series of four different target basal areas of 8, 12, 16 and 20 m2 ha1 (Vesijako and Mikkeli) or 10, 15, 20, and 25 m2 ha1 (Suonenjoki I, II and Evo) (Table 1). In each main plot and stand, subplots are replicated once in two opposed rows in the monitoring plot with buffer zones between rows. In earlier studies (Saksa, 2004; Eerikäinen et al., 2007; Saksa and Valkonen, 2011), diameter at breast height, coordinates, height, vitality and health and malformed or dead crown of each individual was recorded at 5-year intervals. The last tree measurements were taken in 2012 in Evo and Vesijako stands, and in 2013– 2014 in three other stands. Trees on every subplot were divided into eight diameter classes and every third individual from each class was chosen as a sample tree. The upper third of their living crowns were photographed in June 2014 with a digital camera (focal length of 215 mm at maximum, 35 mm film equivalent 1200 mm) with an optical image stabilizer. Current-year cones and cones from the 2012 crop were counted in the photographs (see Supplementary material) using ‘‘ImageJ” (Schneider et al., 2012). Year is referred to as the seed ripening year. In total, 639 trees were photographed. As tree crowns were photographed only from one side, a correction factor given by Machanicek (1973) was used in order to account for the number of cones from the crown’s nonvisible side. An unknown,
but different proportion of 2012 cones in dominant and codominant trees may have been dropped from the crowns by the time we had done our inventory. Thus, generally the number of cones in that year may have been underestimated. 2.1. Statistical analyses In the first step of the analysis of cone crop per tree, a generalized linear model with Poisson distribution and log link was fitted to the data. The dependent variable was the number of currentyear cones in a given individual. The fixed, independent variables were tree diameter at breast height (D), local (subplot) basal area (B), a given stand (S) and a binary dummy variable (C) indicating whether a given individual produced cones two years earlier (at least 20 cones, yes/no). The limit of 20 cones per tree was subjectively chosen to divide the data between flowering and nonflowering individuals. This value is approximately one-third of the mean cone number value in the data. The Poisson model did not fit the data well due to many zerovalued observations. This was indicated by large residual mean deviance 48.36 (30,566 with 632 degrees of freedom). In order to account the large variation in the data, a negative binomial model with an estimated heterogeneity parameter k was used. The fit of this model was satisfactory as indicated by residual mean deviance of 1.092 (690.0 with 632 df). The final model was:
logðlÞ ¼ b0 þ b1 D þ b2 B þ b3 S þ b4 C
ð1Þ
ncones NegBinðl; kÞ Eðncones Þ ¼ l and varðncones Þ ¼ l þ l2 =k where ncones = the number of cones in each individual tree. Overall fit of the model (1) was examined by looking at graphical summaries of the standardized residuals vs. fitted values and covariates. Pearson chi-square test was used to evaluate the observed cone frequency classes vs predicted values from the model (1). Individual model terms were assessed by comparing the log-likelihood statistics of two nested, candidate models and Wald-significance tests for parameter coefficients. Model terms were considered statistically significant at p 6 0.05. For all analyses, Genstat 18 (VSN International...2014) regression procedures were used. 2.2. Analysis of seed quality data To determine the seed crop’s quality, a sample of 162 cones (6 cones per tree on average) was taken from 26 randomly chosen sample trees in Suonenjoki I and II stands. The cones were collected in February 2015. Altogether, 2163 seeds from these samples were X-rayed (Faxitron MX-20, IL, USA, exposure time 18 kV, 4 s; image processing with Agfa CR-30X reader) and classified in three categories: (1) full seeds with properly developed embryos
Table 1 Local basal areas for Norway spruce trees (with diameter at breast height larger than 10 cm) on the multiple density plots in the five experimental stands of the study. Local basal area, m2 ha1 Parameter
Mean
Median
Min.
Max.
Stand Stand Stand Stand Stand
16.6 16.2 20.7 17.3 17.6
17.2 14.2 19.7 18.6 16.0
9.4 9.6 14.6 9.9 12.5
21.9 23.2 27.6 24.4 23.9
1 2 3 4 5
(Evo) (Vesijako) (Suonenjoki I) (Suonenjoki II) (Mikkeli)
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M. Nygren et al. / Forest Ecology and Management 390 (2017) 68–72
and megagametophytes, (2) empty seeds and (3) insect-damaged seeds.
Table 2 Parameter estimates of the model (1). Parameter a
k Constant Diameter Local basal area Cones in 2012 Stand 2 (Vesijako)b Stand 3 (Suonenjoki I) Stand 4 (Suonenjoki II) Stand 5 (Mikkeli)
3. Results There was a large variation in the number of cones between individual trees. Of 639 trees studied, 278 had no cones in the year 2014. Two years earlier, a similar situation was observed: 270 trees had no cones. The average number of cones per tree for trees bearing any cones was 92 in 2014 and 66 in 2012. Median values were 64 and 48, respectively. Highest cone numbers found per individual tree were 526 in the year 2014 and 364 in the year 2012. Of all trees studied, 55.5% produced cones for both years, 9.6% produced cones once and 34.9% did not produce cones in 2012 or 2014. The frequency distribution of the cone counts per tree was highly skewed to the right (Fig. 1). Median cone count values predicted with the model (1) were higher (23.5) than those observed (17.6) and the predicted values did not totally agree with the observed data (Likelihood chi-square = 75.46 on 4 d.f., p < 0.001). However, we considered the overall fit of the model (1) satisfactory, as indicated by the dispersion statistic value of 1.09, i.e. close to 1 as in an ideally fitted Poisson or negative binomial generalized linear model (cf. Zuur et al., 2013, p. 27). The number of cones per tree in 2014 was positively correlated with tree diameter at breast height and negatively correlated with local basal area when inspected using the model (1) (Tables 2 and 3). Further, the number of cones was positively correlated with presence of cones (at least twenty) in that particular individual two years earlier (Table 2, Fig. 2). Also, the stand effects were statistically significant indicating acclimation of cone and seed production with local environmental conditions. The quality of the seed crop in 2014 as determined in stands I and II in Suonenjoki was poor. Of all seeds X-rayed, 44% were empty, 29% were damaged by insects feeding on seeds (Plemeliella abietina or Megastigmus strobilobius) and only 25% were full and capable of germination.
a b
Estimate
s.e.
t-value
0.3756 0.219 0.1971 0.0849 0.894 0.618 1.257 0.780 0.992
0.322 0.0105 0.0152 0.171 0.216 0.263 0.211 0.213
0.497 <0.001 <0.001 <0.001 0.004 <0.001 <0.001 <0.001
Extra variation parameter in the negative binomial distribution. Values of stand parameters compared to reference level (Stand 1, Evo).
Table 3 Predicted mean cone count (±s.e.) per individual Norway spruce tree in 2014 as a function of breast height diameter at two local basal area levels according to model (1). Standard errors are approximate since the model is not linear. Local basal area m2 ha1 Diameter, cm
10
20
15 20 25 30 35
15.6 (2.5) 38.2 (5.5) 93.5 (13.7) 228.9 (38.3) 560.4 (111.9)
6.7 (0.9) 16.3 (1.7) 40.0 (3.5) 98.0 (9.7) 239.9 (31.9)
Fig. 2. Predicted mean number of cones in an individual tree in 2014 as a function of breast height diameter and whether or not the tree had produced cones two years earlier. Model (1) predictions are based on an average local basal area of 17.4 m2 ha1. Standard errors are approximate since the model is not linear.
4. Discussion
Fig. 1. Frequency distribution of the number of cones per tree. Observed data vs. fitted values of model (1).
Approximately a third of the trees in our study had at least twenty cones in both years. Neither of the years can be regarded as an abundant crop year. As shown by Annila (1981), individual mature Norway spruce trees can have as many as 800 cones in a masting year and nearly three-quarters of the trees have more than 100 cones. In years of poor cone production, most trees have less than a hundred cones. High cone count values in individual trees in masting years have been reported by Mälkönen (1971, 1123 cones) and Rummukainen (1956, 886 cones). For a general survey of the Norway spruce cone crop survey in southern Finland, mean values per tree were 85 cones in 2012 and 79 cones in 2014 (Zamorano et al., 2016). These values are close to those found in this study, also.
M. Nygren et al. / Forest Ecology and Management 390 (2017) 68–72
The positive correlation between the breast height diameter and the number of cones in individual Norway spruce trees has been well documented in previous literature (Heikinheimo, 1932; Tiren, 1951; Mälkönen, 1971). Hagner (1957) reported that Norway spruce trees with a breast height diameter of 40 cm produced about twice as many cones as trees with a diameter of 25 cm. Considering the large variation in cone count data in general, the predicted number of cone values in our study were in line with those estimated in earlier studies. Saksa (2004) compared average annual Norway spruce seed crops in five uneven-aged stands to crops in a single even-aged spruce stand located in the same geographical area in southern Finland for the years 1990–2001. The annual fluctuation of seed crops in uneven-aged stands was similar to that in an even-aged stand. Yet, the amount of seeds produced in uneven-aged stands was only approximately half of that in an even-aged stand. This was attributed to fewer large trees (diameter at breast height >25 cm) in uneven-aged stands. According to Koski and Tallqvist (1978), in even-aged stands, when the number of large spruce stems increased from 200 to 500 stems ha1, stand seed production capacity increased threefold. The tendency of some Norway spruce individuals to flowering and producing abundant crops more often than others is well known in forest stands (Koski and Tallqvist, 1978; Annila, 1981) and in seed orchards (Nikkanen and Ruotsalainen, 2000). Based on our results, we conclude that, when looking at cone-crop production history, individuals that are more prone to flowering can be detected. In our study, trees that had flowered in 2012, produced, on average, twice as many cones than those that did not flower (Fig. 2). Similarly, Hagner (1965a) found that the best method for selecting trees with rich future seed production was to monitor the number of cones they produced in the preceding years. According to Annila (1981), there is a positive correlation between the frequency of flowering and the number of female flowers. Some individuals even produce cones in scarce flowering years; in rich years, these individuals exhibit above average cone production. In years of low seed set, only the trees that flower abundantly in rich years produce any seeds. Our results regarding the effects of local basal area on individual trees’ cone crop match the hypothesis of Saksa (2004), suggesting that a wider spacing of trees in an uneven-aged stand creates favorable environmental conditions for the initiation of female flower buds and cone production. This was evident in our study, for the number of cones produced per individual tree correlated negatively with local basal area (Table 3). Reukema (1982) found that during a 29-year monitoring of seedfall in a Douglas fir stand, thinning substantially increased the number of seeds produced after thinning, but the effect was not lasting. He suggested favoring selected seed trees by removing approximately a third of the basal area in surrounding trees in order to increase seed production in the next adequate year by at least 50% and probably more. Yet, the wide spacing of mature, cone-bearing trees in unevenaged stands could increase the percentage of empty seeds due to insufficient pollination (Sarvas, 1957; Neale and Adams, 1985; Smith et al., 1988) and the percentage of self-fertilized offspring as suggested by Rudin et al. (1977) in research on the Scots pine. In this study, a small random sample taken from two stands indicated that only 25% of the seeds were full and germinable, whereas the rest were empty or damaged by insects. According to Sarvas (1968), in Norway spruce mast years when the density of the pollen cloud in stands is at its highest, the percentage of empty seeds typically varies between 3 and 6%. In years of poor flowering and low pollen production, the proportion of empty seeds ranges from 30 to 90%. It appears that high-quality
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spruce seed crops are only available during years of abundant flowering and large cone crops. It remains to be determined if trees in uneven-aged stands behave differently in this respect than those in even-aged stands. As the data collected for this study covers on two years, flowering and seed development in individual trees growing in both management regimes should be followed over a longer timer period and especially, during a mast year. Digital cone count using photographs proved to be a useful method. Previously, counting has been done with binoculars from the ground, and the results have been expressed as cone number classes or merely classifications such as ‘‘poor, medium, good and full” crop (Hagner, 1965b; Barner and Olesen, 1994). This is a subjective technique, and its accuracy is dependent on weather conditions, tree density, researcher skill, etc. The technique presented in this study is more accurate and allows for an exact count, even if cone numbers are high. Based on color differences between new (greenish and yellow- greenish) and old cones (dark brown), it was possible to separate the 2014 crop from the crop two years earlier (see Supplementary photograph). We concluded that all brown cones really represented the crop from 2012, as spruce flowering was very poor in general in 2013 (Zamorano et al., 2016). Although it was not possible to cut down sample trees for cone count verification in this study, we compared the results of automatic counting using ‘‘ImageJ” to manual counting based on the photographs. Kendall’s rank correlation between these two was 0.896, indicating good agreement. In future studies, however, results of automatic counting from crown photographs should be verified against data from felled sample trees. Our results have implications for management practices in uneven-aged Norway spruce stands. We suggest that, at each harvest entry, at least some large, prolific trees should be retained in order to increase the total number of seeds produced in a stand for regeneration and the recruitment of new seedlings. According to Hagner (1965a), by removing the largest and most valuable seed trees, and leaving only the smallest 25% of the seed tree candidates, future cone production may be decreased by up to 50% of what it might have been if an equal number of the current, most cone producing trees were left. In terms of increasing the potential for more regular, abundant crops, attention should be concentrated on leaving tall trees with crop production history to serve as seed trees. Acknowledgements We thank Pekka Helminen, Hilkka Ollikainen and Juhani Korhonen for their assistance in locating the sample plots and mapping sample trees as well as Tarja Salminen and Jussi Tiainen for their assistance in collecting the cones samples. Appendix A. Supplementary material Supplementary data associated with this article can be found, in the online version, at http://dx.doi.org/10.1016/j.foreco.2017.01. 016. References Almqvist, C., Bergsten, U., Bondesson, L., Eriksson, U., 1998. Predicting germination capacity of Pinus sylvestris and Picea abies seeds using temperature data from weather stations. Can. J. For. Res. 28, 1530–1535. Andersson, E., 1965. Cone and seed studies in Norway spruce. Stud. For. Suec. Nr 23. Annila, E., 1981. Kuusen käpy- ja siementuholaisten kannanvaihtelu. Summary: Fluctuations in cone and seed insect populations in Norway spruce. Comm. Inst. For. Fenniae, vol. 101. Barner, H., Olesen, K., 1994. Seed crop evaluation. Danida Forest Seed Centre, Technical Note No. 19. Revised version, April 1994. ISSN 0902–3224. Eerikäinen, K., Miina, J., Valkonen, S., 2007. Models for the regeneration establishment and development of established seedlings in uneven-aged
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Norway spruce dominated forest stands in southern Finland. For. Ecol. Manage. 242, 444–461. Hagner, S., 1957. Om kott- och fröproduktionen i svenska barrskogar. Medd. Stat. Skogsforskn. Inst. 47, 8. Hagner, S., 1965a. Om fröproduktion, fröträdsval och plantuppslag i försök med naturlig föryngring. Yield of seed, choice of seed trees, and seedling establishment in experiments with natural regeneration. Stud. For. Suec., Nr. 27. Hagner, S., 1965b. Om variation och stickprovstorlek vid uppmätning av fröfall, kottinsättning och taxering av plantuppslag. Variation and size of the random samples when measuring seed fall, cone setting, and stocking. Stud. For. Suec., Nr. 28. Heikinheimo, O., 1932. Metsäpuiden siementämiskyvystä. Comm. Inst. For. Fenniae 17, 3. Hokkanen, T., 2000. Seed crops and seed crop forecasts for a number of tree species. In: Mälkönen, E., Babich, N., Krutov, V., Markova, I., (Eds.), Forest Regeneration in the Northern Parts of Europe. Finnish Forest Research Institute, Research Papers 790, pp. 87–97. Koski, V., Tallqvist, R., 1978. Tuloksia monivuotisista kukinnan ja siemensadon määrän mittauksista metsäpuilla. Results of long-time measurements of flowering and seed crop of forest trees. Folia For., vol. 364. Machanicek, J., 1973. Economic collection of cones of forest conifers on the basis of preceding estimation of cone crop. In: International Symposium on Seed Processing, IUFRO Working Party S2.01.06 ‘Seed Problems’. Bergen, Norway. 22 p. Mälkönen, E., 1971. Fertilizer treatment and seed crop of Picea abies. Comm. Inst. For. Fenniae 73, 4. Neale, D.B., Adams, W.T., 1985. The mating system in natural and shelterwood stands of Douglas-fir. Theor. Appl. Genet. 71, 201–207. Nikkanen, T., Ruotsalainen, S., 2000. Variation in flowering abundance and its impact on the genetic diversity of the seed crop in a Norway spruce seed orchard. Silva Fenn. 34 (3), 205–222. Opsahl, W., 1952. Om sambandet mellom sommertemperatur og frömodning hos gran. On Relations between Summer Temperature and Seed Ripening of Norway spruce. Medd. Norske Skogforsöksvesen 40, 623–662. Pukkala, T., Hokkanen, T., Nikkanen, T., 2010. Prediction models for the annual seed crop of Norway spruce and Scots pine in Finland. Silva Fenn. 44 (4), 629–642. Reukema, D.L., 1982. Seedfall in a young-growth Douglas-fir stand: 1950–1978. Can. J. For. Res. 12, 249–254.
Rudin, D., Eriksson, G., Rasmuson, M., 1977. Inbreeding in a seed tree stand of Pinus sylvestris L. in northern Sweden. A study by the aid of the isozyme technique. Dept. of Forest Genetics, Royal College of Forestry. Research note 25. Rummukainen, U., 1956. Käpysadon arvioinnista. Über die Abschätzung der Zapfenernte. Comm. Inst. For. Fenniae 46 (7). Saksa, T., 2004. Regeneration process from seed crop to saplings – a case study in uneven-aged Norway spruce-dominated stands in southern Finland. Silva Fenn. 38 (4), 371–381. Saksa, T., Valkonen, S., 2011. Dynamics of seedling establishment and survival in uneven-aged boreal forests. For. Ecol. Manage. 261, 1409–1414. Sarvas, R., 1957. Studies on the seed setting of Norway spruce. Medd. Norske Skogforsöksvesen Nr. 48. Sarvas, R., 1968. Investigations on the flowering and seed crop of Picea abies. Comm. Inst. For. Fenniae 67, 5. Schneider, C.A., Rasband, W.S., Eliceiri, K.W., 2012. NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 9 (7), 671–675. Silvertown, J.W., 1980. The evolutionary ecology of mast seeding in trees. Biol. J. Linn. Soc. 14, 235–250. Smith, C.C., Hamrick, J.L., Kramer, C.L., 1988. The effects of stand density of the frequency of filled seeds and fecundity in lodgepole pine (Pinus contorta Dougl.). Can. J. For. Res. 18, 453–460. Tiren, L., 1935. Om granens kottsättning, des periodicitet och samband med temperatur och nederbörd. Medd. Stat. Skogsforskn Inst. 28, 413–518. Tiren, L., 1951. Om hyggesgranen och dess betydelse för de norrländska granskogens föryngring. On clearing-spruce and its significance to the reforestation of spruce forest clearings in northern Sweden. Medd. Stat. Skogsforskn. Inst. 39 (8). Valkonen, S., Maguire, D., 2005. Relationship between seedbed properties and the emergence of spruce germinants in recently cut Norway spruce selection stands in Southern Finland. For. Ecol. Manage. 210, 255–266. VSN International, 2014. GenStat for Windows 17th Edition. VSN International, Hemel Hempstead, UK. Web page: GenStat.co.uk. Waldron, R.M., 1965. Cone production and seedfall in a mature white spruce stand. Forest. Chron. 41, 314–329. Zamorano, J.G., Hokkanen, T., Lehikoinen, A., 2016. Climate-driven synchrony in seed production of masting deciduous and conifer tree species. J. Plant Ecol. http://dx.doi.org/10.1093/jpe/rtw117. Zuur, A.F., Hilbe, J.M., Ieno, E.N., 2013. A Beginner Guide to GLM and GLMM with R. A frequentist and Bayesian perspective for ecologists. Highland Statistics Ltd. ISBN: 978-0-9571741-3-9.
Contents lists available at ScienceDirect
Forest Ecology and Management journal homepage: www.elsevier.com/locate/foreco
Norway spruce cone crops in uneven-aged stands in southern Finland: A case study Markku Nygren a,⇑, Kaisa Rissanen b, Kalle Eerikäinen c, Timo Saksa a, Sauli Valkonen d a
Natural Resources Institute Finland, Suonenjoki Unit, Juntintie 154, FI-77600 Suonenjoki, Finland Department of Forest Sciences, University of Helsinki, P.O. Box 27, FI-00014, Finland c Suomen Sijoitusmetsät Oy, Länsikatu 15, FI-80110 Joensuu, Finland d Natural Resources Institute Finland, Latokartanonkaari 9, FI-00790 Helsinki, Finland b
a r t i c l e
i n f o
Article history: Received 15 December 2016 Received in revised form 13 January 2017 Accepted 16 January 2017
Keywords: Picea abies (L.) Seeds Flowering Regeneration Uneven-aged management Image analysis
a b s t r a c t Norway spruce cone crops in individual trees from two seed ripening years 2012 and 2014 were studied. Data were collected from five stands in southern Finland, managed by single-tree selection harvests since the 1980s. The upper third of living crown of each individual tree was photographed for digital cone counting with image analysis. The average number of cones per tree for trees bearing any cones was 92 in 2014 and 66 in 2012. Highest cone numbers found per individual tree were 526 in the year 2014 and 364 in the year 2012. Of all trees studied, 55.5% produced cones during both years, 9.6% produced cones once and 34.9% did not produce cones in 2012 or 2014. The number of cones per tree in 2014 was positively correlated with tree diameter at breast height and the presence of cones (at least twenty) in that particular individual two years earlier and negatively correlated with local basal area. The quality of the seed crop in 2014 as determined in two of the stands was poor. Based on X-ray analyses, 44% of seeds were empty, 29% were damaged by insects feeding on seeds (Plemeliella abietina or Megastigmus strobilobius) and only 25% were full and capable of germination. The results have implications for management practices in uneven-aged Norway spruce stands. It is suggested that at each harvest entry, some large, prolific trees should be retained in order to increase the total number of seeds produced in a stand to enhance regeneration and the recruitment of new seedlings. Ó 2017 Elsevier B.V. All rights reserved.
1. Introduction Norway spruce in Fennoscandia shows high year-to-year variation in cone and seed production. In southern Finland, for example, abundant cone crops generally occur only once or twice a decade. In northern Finland, good cone crops are even less frequent (Tiren, 1935; Sarvas, 1957; Koski and Tallqvist, 1978; Pukkala et al., 2010) and seed maturation in this region may be incomplete due to harsh climatic conditions (Opsahl, 1952; Almqvist et al., 1998). Furthermore, Norway spruce seed crops are often of poor quality, as seeds are frequently destroyed by insects (Hokkanen, 2000). Also, in poor flowering years, the number of empty Norway spruce seeds is high, ranging from 50 to 90% (Andersson, 1965; Sarvas, 1968). Historically, Norway spruce cone and seed crops have been intensively studied in all Nordic countries, though older informa-
⇑ Corresponding author. E-mail addresses: [email protected] (M. Nygren), [email protected] (K. Rissanen), [email protected] (K. Eerikäinen), [email protected] (T. Saksa), [email protected] (S. Valkonen). http://dx.doi.org/10.1016/j.foreco.2017.01.016 0378-1127/Ó 2017 Elsevier B.V. All rights reserved.
tion is based on data from trees growing in even-aged stands. The results of these studies may not be directly applicable to selection stands because of different stem counts, basal area and stand structure in uneven-aged stands (Valkonen and Maguire, 2005). Norway spruce cone and seed crops are also characterized by large variations between individual trees in a stand. The percentage trees that flower varies, depending on whether it is an abundant or scarce flowering year. Koski and Tallqvist (1978) found that in abundant flowering years, the percentage of nonflowering trees is between 2 and 10%, whereas during the years of scarce flowering, this percentage is 55–98%. Thus, only a small part of the trees may produce the bulk of cone and seed crops, particularly in poor seed years. During a 12-year monitoring period, in an 80year-old, even-aged Norway spruce stand in southern Finland, 20% of individuals produced 50% of the total cone crop (Annila, 1981). Generally, dominant and codominant trees produce heavier and more frequent cone crops than intermediate trees; the latter, in turn, produce heavier and more frequent crops than suppressed trees (Heikinheimo, 1932; Waldron, 1965). Moreover, both cone
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size and the number of seeds in an individual cone are positively correlated with tree size (Heikinheimo, 1932; Andersson, 1965). The high year-to-year variation in cone and seed production of Norway spruce presents a challenge to all types of natural regeneration of spruce stands. Synchronous production of large seed crops followed by small seed crops, ie. masting (Silvertown, 1980) has special implications on selection stands with generally continuous seed production as well as the establishment of new seedlings are required for sustainable management. The objective of this case study was to examine the quantity and quality of cone and seed crop in individual Norway spruce trees in stands managed with single-tree selection.
2. Material and methods The data for this study was collected from permanent sample plots established by the Finnish Forest Research Institute (nowadays Natural Resources Institute Finland), in five stands dominated by Norway spruce in southern Finland and managed by single-tree selection harvests since the 1980s. The stands represent samples of either distinct selection structures due to past selection treatments or different stages of transition from an irregular structure towards some, yet unknown, sustainable selection structure (Saksa and Valkonen, 2011). The area of each stand was about 2 ha. They were grown on mineral soils, and the forest site type was either mesic OxalisMyrtillus or submesic Myrtillus type. Specifically, we used the multiple density plots (cf. Eerikäinen et al., 2007) established in these stands from 1992–1994. These plots are rectangular (80 m 100 m) areas, each divided into 8 subplots (20 20 m) with 10-m buffer zones. Subplots form a series of four different target basal areas of 8, 12, 16 and 20 m2 ha1 (Vesijako and Mikkeli) or 10, 15, 20, and 25 m2 ha1 (Suonenjoki I, II and Evo) (Table 1). In each main plot and stand, subplots are replicated once in two opposed rows in the monitoring plot with buffer zones between rows. In earlier studies (Saksa, 2004; Eerikäinen et al., 2007; Saksa and Valkonen, 2011), diameter at breast height, coordinates, height, vitality and health and malformed or dead crown of each individual was recorded at 5-year intervals. The last tree measurements were taken in 2012 in Evo and Vesijako stands, and in 2013– 2014 in three other stands. Trees on every subplot were divided into eight diameter classes and every third individual from each class was chosen as a sample tree. The upper third of their living crowns were photographed in June 2014 with a digital camera (focal length of 215 mm at maximum, 35 mm film equivalent 1200 mm) with an optical image stabilizer. Current-year cones and cones from the 2012 crop were counted in the photographs (see Supplementary material) using ‘‘ImageJ” (Schneider et al., 2012). Year is referred to as the seed ripening year. In total, 639 trees were photographed. As tree crowns were photographed only from one side, a correction factor given by Machanicek (1973) was used in order to account for the number of cones from the crown’s nonvisible side. An unknown,
but different proportion of 2012 cones in dominant and codominant trees may have been dropped from the crowns by the time we had done our inventory. Thus, generally the number of cones in that year may have been underestimated. 2.1. Statistical analyses In the first step of the analysis of cone crop per tree, a generalized linear model with Poisson distribution and log link was fitted to the data. The dependent variable was the number of currentyear cones in a given individual. The fixed, independent variables were tree diameter at breast height (D), local (subplot) basal area (B), a given stand (S) and a binary dummy variable (C) indicating whether a given individual produced cones two years earlier (at least 20 cones, yes/no). The limit of 20 cones per tree was subjectively chosen to divide the data between flowering and nonflowering individuals. This value is approximately one-third of the mean cone number value in the data. The Poisson model did not fit the data well due to many zerovalued observations. This was indicated by large residual mean deviance 48.36 (30,566 with 632 degrees of freedom). In order to account the large variation in the data, a negative binomial model with an estimated heterogeneity parameter k was used. The fit of this model was satisfactory as indicated by residual mean deviance of 1.092 (690.0 with 632 df). The final model was:
logðlÞ ¼ b0 þ b1 D þ b2 B þ b3 S þ b4 C
ð1Þ
ncones NegBinðl; kÞ Eðncones Þ ¼ l and varðncones Þ ¼ l þ l2 =k where ncones = the number of cones in each individual tree. Overall fit of the model (1) was examined by looking at graphical summaries of the standardized residuals vs. fitted values and covariates. Pearson chi-square test was used to evaluate the observed cone frequency classes vs predicted values from the model (1). Individual model terms were assessed by comparing the log-likelihood statistics of two nested, candidate models and Wald-significance tests for parameter coefficients. Model terms were considered statistically significant at p 6 0.05. For all analyses, Genstat 18 (VSN International...2014) regression procedures were used. 2.2. Analysis of seed quality data To determine the seed crop’s quality, a sample of 162 cones (6 cones per tree on average) was taken from 26 randomly chosen sample trees in Suonenjoki I and II stands. The cones were collected in February 2015. Altogether, 2163 seeds from these samples were X-rayed (Faxitron MX-20, IL, USA, exposure time 18 kV, 4 s; image processing with Agfa CR-30X reader) and classified in three categories: (1) full seeds with properly developed embryos
Table 1 Local basal areas for Norway spruce trees (with diameter at breast height larger than 10 cm) on the multiple density plots in the five experimental stands of the study. Local basal area, m2 ha1 Parameter
Mean
Median
Min.
Max.
Stand Stand Stand Stand Stand
16.6 16.2 20.7 17.3 17.6
17.2 14.2 19.7 18.6 16.0
9.4 9.6 14.6 9.9 12.5
21.9 23.2 27.6 24.4 23.9
1 2 3 4 5
(Evo) (Vesijako) (Suonenjoki I) (Suonenjoki II) (Mikkeli)
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and megagametophytes, (2) empty seeds and (3) insect-damaged seeds.
Table 2 Parameter estimates of the model (1). Parameter a
k Constant Diameter Local basal area Cones in 2012 Stand 2 (Vesijako)b Stand 3 (Suonenjoki I) Stand 4 (Suonenjoki II) Stand 5 (Mikkeli)
3. Results There was a large variation in the number of cones between individual trees. Of 639 trees studied, 278 had no cones in the year 2014. Two years earlier, a similar situation was observed: 270 trees had no cones. The average number of cones per tree for trees bearing any cones was 92 in 2014 and 66 in 2012. Median values were 64 and 48, respectively. Highest cone numbers found per individual tree were 526 in the year 2014 and 364 in the year 2012. Of all trees studied, 55.5% produced cones for both years, 9.6% produced cones once and 34.9% did not produce cones in 2012 or 2014. The frequency distribution of the cone counts per tree was highly skewed to the right (Fig. 1). Median cone count values predicted with the model (1) were higher (23.5) than those observed (17.6) and the predicted values did not totally agree with the observed data (Likelihood chi-square = 75.46 on 4 d.f., p < 0.001). However, we considered the overall fit of the model (1) satisfactory, as indicated by the dispersion statistic value of 1.09, i.e. close to 1 as in an ideally fitted Poisson or negative binomial generalized linear model (cf. Zuur et al., 2013, p. 27). The number of cones per tree in 2014 was positively correlated with tree diameter at breast height and negatively correlated with local basal area when inspected using the model (1) (Tables 2 and 3). Further, the number of cones was positively correlated with presence of cones (at least twenty) in that particular individual two years earlier (Table 2, Fig. 2). Also, the stand effects were statistically significant indicating acclimation of cone and seed production with local environmental conditions. The quality of the seed crop in 2014 as determined in stands I and II in Suonenjoki was poor. Of all seeds X-rayed, 44% were empty, 29% were damaged by insects feeding on seeds (Plemeliella abietina or Megastigmus strobilobius) and only 25% were full and capable of germination.
a b
Estimate
s.e.
t-value
0.3756 0.219 0.1971 0.0849 0.894 0.618 1.257 0.780 0.992
0.322 0.0105 0.0152 0.171 0.216 0.263 0.211 0.213
0.497 <0.001 <0.001 <0.001 0.004 <0.001 <0.001 <0.001
Extra variation parameter in the negative binomial distribution. Values of stand parameters compared to reference level (Stand 1, Evo).
Table 3 Predicted mean cone count (±s.e.) per individual Norway spruce tree in 2014 as a function of breast height diameter at two local basal area levels according to model (1). Standard errors are approximate since the model is not linear. Local basal area m2 ha1 Diameter, cm
10
20
15 20 25 30 35
15.6 (2.5) 38.2 (5.5) 93.5 (13.7) 228.9 (38.3) 560.4 (111.9)
6.7 (0.9) 16.3 (1.7) 40.0 (3.5) 98.0 (9.7) 239.9 (31.9)
Fig. 2. Predicted mean number of cones in an individual tree in 2014 as a function of breast height diameter and whether or not the tree had produced cones two years earlier. Model (1) predictions are based on an average local basal area of 17.4 m2 ha1. Standard errors are approximate since the model is not linear.
4. Discussion
Fig. 1. Frequency distribution of the number of cones per tree. Observed data vs. fitted values of model (1).
Approximately a third of the trees in our study had at least twenty cones in both years. Neither of the years can be regarded as an abundant crop year. As shown by Annila (1981), individual mature Norway spruce trees can have as many as 800 cones in a masting year and nearly three-quarters of the trees have more than 100 cones. In years of poor cone production, most trees have less than a hundred cones. High cone count values in individual trees in masting years have been reported by Mälkönen (1971, 1123 cones) and Rummukainen (1956, 886 cones). For a general survey of the Norway spruce cone crop survey in southern Finland, mean values per tree were 85 cones in 2012 and 79 cones in 2014 (Zamorano et al., 2016). These values are close to those found in this study, also.
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The positive correlation between the breast height diameter and the number of cones in individual Norway spruce trees has been well documented in previous literature (Heikinheimo, 1932; Tiren, 1951; Mälkönen, 1971). Hagner (1957) reported that Norway spruce trees with a breast height diameter of 40 cm produced about twice as many cones as trees with a diameter of 25 cm. Considering the large variation in cone count data in general, the predicted number of cone values in our study were in line with those estimated in earlier studies. Saksa (2004) compared average annual Norway spruce seed crops in five uneven-aged stands to crops in a single even-aged spruce stand located in the same geographical area in southern Finland for the years 1990–2001. The annual fluctuation of seed crops in uneven-aged stands was similar to that in an even-aged stand. Yet, the amount of seeds produced in uneven-aged stands was only approximately half of that in an even-aged stand. This was attributed to fewer large trees (diameter at breast height >25 cm) in uneven-aged stands. According to Koski and Tallqvist (1978), in even-aged stands, when the number of large spruce stems increased from 200 to 500 stems ha1, stand seed production capacity increased threefold. The tendency of some Norway spruce individuals to flowering and producing abundant crops more often than others is well known in forest stands (Koski and Tallqvist, 1978; Annila, 1981) and in seed orchards (Nikkanen and Ruotsalainen, 2000). Based on our results, we conclude that, when looking at cone-crop production history, individuals that are more prone to flowering can be detected. In our study, trees that had flowered in 2012, produced, on average, twice as many cones than those that did not flower (Fig. 2). Similarly, Hagner (1965a) found that the best method for selecting trees with rich future seed production was to monitor the number of cones they produced in the preceding years. According to Annila (1981), there is a positive correlation between the frequency of flowering and the number of female flowers. Some individuals even produce cones in scarce flowering years; in rich years, these individuals exhibit above average cone production. In years of low seed set, only the trees that flower abundantly in rich years produce any seeds. Our results regarding the effects of local basal area on individual trees’ cone crop match the hypothesis of Saksa (2004), suggesting that a wider spacing of trees in an uneven-aged stand creates favorable environmental conditions for the initiation of female flower buds and cone production. This was evident in our study, for the number of cones produced per individual tree correlated negatively with local basal area (Table 3). Reukema (1982) found that during a 29-year monitoring of seedfall in a Douglas fir stand, thinning substantially increased the number of seeds produced after thinning, but the effect was not lasting. He suggested favoring selected seed trees by removing approximately a third of the basal area in surrounding trees in order to increase seed production in the next adequate year by at least 50% and probably more. Yet, the wide spacing of mature, cone-bearing trees in unevenaged stands could increase the percentage of empty seeds due to insufficient pollination (Sarvas, 1957; Neale and Adams, 1985; Smith et al., 1988) and the percentage of self-fertilized offspring as suggested by Rudin et al. (1977) in research on the Scots pine. In this study, a small random sample taken from two stands indicated that only 25% of the seeds were full and germinable, whereas the rest were empty or damaged by insects. According to Sarvas (1968), in Norway spruce mast years when the density of the pollen cloud in stands is at its highest, the percentage of empty seeds typically varies between 3 and 6%. In years of poor flowering and low pollen production, the proportion of empty seeds ranges from 30 to 90%. It appears that high-quality
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spruce seed crops are only available during years of abundant flowering and large cone crops. It remains to be determined if trees in uneven-aged stands behave differently in this respect than those in even-aged stands. As the data collected for this study covers on two years, flowering and seed development in individual trees growing in both management regimes should be followed over a longer timer period and especially, during a mast year. Digital cone count using photographs proved to be a useful method. Previously, counting has been done with binoculars from the ground, and the results have been expressed as cone number classes or merely classifications such as ‘‘poor, medium, good and full” crop (Hagner, 1965b; Barner and Olesen, 1994). This is a subjective technique, and its accuracy is dependent on weather conditions, tree density, researcher skill, etc. The technique presented in this study is more accurate and allows for an exact count, even if cone numbers are high. Based on color differences between new (greenish and yellow- greenish) and old cones (dark brown), it was possible to separate the 2014 crop from the crop two years earlier (see Supplementary photograph). We concluded that all brown cones really represented the crop from 2012, as spruce flowering was very poor in general in 2013 (Zamorano et al., 2016). Although it was not possible to cut down sample trees for cone count verification in this study, we compared the results of automatic counting using ‘‘ImageJ” to manual counting based on the photographs. Kendall’s rank correlation between these two was 0.896, indicating good agreement. In future studies, however, results of automatic counting from crown photographs should be verified against data from felled sample trees. Our results have implications for management practices in uneven-aged Norway spruce stands. We suggest that, at each harvest entry, at least some large, prolific trees should be retained in order to increase the total number of seeds produced in a stand for regeneration and the recruitment of new seedlings. According to Hagner (1965a), by removing the largest and most valuable seed trees, and leaving only the smallest 25% of the seed tree candidates, future cone production may be decreased by up to 50% of what it might have been if an equal number of the current, most cone producing trees were left. In terms of increasing the potential for more regular, abundant crops, attention should be concentrated on leaving tall trees with crop production history to serve as seed trees. Acknowledgements We thank Pekka Helminen, Hilkka Ollikainen and Juhani Korhonen for their assistance in locating the sample plots and mapping sample trees as well as Tarja Salminen and Jussi Tiainen for their assistance in collecting the cones samples. Appendix A. Supplementary material Supplementary data associated with this article can be found, in the online version, at http://dx.doi.org/10.1016/j.foreco.2017.01. 016. References Almqvist, C., Bergsten, U., Bondesson, L., Eriksson, U., 1998. Predicting germination capacity of Pinus sylvestris and Picea abies seeds using temperature data from weather stations. Can. J. For. Res. 28, 1530–1535. Andersson, E., 1965. Cone and seed studies in Norway spruce. Stud. For. Suec. Nr 23. Annila, E., 1981. Kuusen käpy- ja siementuholaisten kannanvaihtelu. Summary: Fluctuations in cone and seed insect populations in Norway spruce. Comm. Inst. For. Fenniae, vol. 101. Barner, H., Olesen, K., 1994. Seed crop evaluation. Danida Forest Seed Centre, Technical Note No. 19. Revised version, April 1994. ISSN 0902–3224. Eerikäinen, K., Miina, J., Valkonen, S., 2007. Models for the regeneration establishment and development of established seedlings in uneven-aged
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