RIS312420 bijlage 4

Jack pine had the highest LMR but lowest SMR while aspen had the smallest LMR but highest SMR. Both LMR and SMR were significantly higher for black spruce than for white spruce. 4

According to Pregitzer et al. (2000), soil temperature can influence the functioning of roots in many ways. If soil moisture and nutrient availability are adequate, rates of root length extension and root mortality increase with increasing soil temperature, at least up to an optimal temperature for root growth, which seems to vary among taxa. Root growth and root mortality are highly seasonal in perennial plants, with a flush of growth in spring and significant mortality in the fall. At present we do not understand whether root growth phenology responds to the same temperature cues that are known to control shoot growth. We also do not understand whether the flush of root growth in the spring depends on the utilization of stored nonstructural carbohydrates, or if it is fueled by current photosynthate. Root respiration increases exponentially with temperature, but Q10 values range widely from c. 1.5 to ¿ 3.0. Significant questions yet to be resolved are: whether rates of root respiration acclimate to soil temperature, and what mechanisms control acclimation if it occurs. Limited data suggest that fine roots depend heavily on the import of new carbon (C) from the canopy during the growing season. We hypothesize that root growth and root respiration are tightly linked to whole-canopy assimilation through complex source–sink relationships within the plant.

Our understanding of how the whole plant responds to dynamic changes in soil temperature, moisture and nutrient availability is poor, even though it is well known that multiple growth-limiting resources change simultaneously through time during a typical growing season. The authors review the interactions between soil temperature and other growth-limiting factors to illustrate how simple generalizations about temperature and root functioning can be misleading. Heninger and White (1974) investigated the effect of soil temperature on shoot and root development for three conifers and two broadleaved species. Plants were raised from seed through two 8-week stages in environmental chambers with soil temperatures controlled in constant-temperature water baths. Soil temperatures were 15, 19, 23, 27, and 31o C and soil moisture between 0.1 and 1.5 bars soil water suction. Other environmental factors were held constant at simulated natural levels. White spruce and tree-of-heaven had optimal shoot and root growth at 19o C. Jack pine growth was maximum at 27o C. Douglas-fir seedlings developed well between 15 and 27o C. Paper birch grew well between 19 and 31o C with best shoot development at 31o C, whereas root development was favored at 23o C. Domisch et al.

(2001) studied effects of soil temperature on shoot and root extension growth and biomass and carbohydrate allocation in Scots pine (Pinus sylvestris L.) seedlings at the beginning of the growing season. One-year-old Scots pine seedlings were grown for 9 weeks at soil temperatures of 5, 9, 13 and 17 o C and an air temperature of 17 o C. Date of bud burst, and the elongation of shoots and roots were monitored. Biomass of current and previous season roots, stem and needles was determined at 3-week intervals. Starch, sucrose, glucose, fructose, sorbitol and inositol concentrations were determined in all plant parts except new roots. The timing of both bud burst and the onset of root elongation were unaffected by soil temperature. At Week 9, height growth was reduced and root extension growth was much less at a soil temperature of 5 o C than at higher soil temperatures. Total seedling biomass was lowest in the 5 o C soil temperature treatment and highest in the 13 o C treatment, but there was no statistically significant difference in total biomass between seedlings grown at 13 and 17 o C. In response to increasing soil temperature, belowground biomass increased markedly, resulting in a slightly higher allocation of biomass to belowground parts. Among treatments, root length was greatest at a soil temperature of 17 o C.

The sugar content of old roots was unaffected by soil temperature, but the sugar content of new needles increased with increasing 5

soil temperature. The starch content of all seedling parts was lowest in seedlings grown at 17 o C. Otherwise, soil temperature had no effect on seedling starch content. Ceccon et al. (2011) identified the role of various soil parameters and root density as drivers of soil respiration (Rs ) in an apple orchard, measured during different periods of the year and at a range of distances from trees, in plots with a different history of nutrient supply. Rs was measured in April, May, August and December and studied in relation to soil temperature and moisture, total soil C and N, as well as to fine root density and medium-, and large-sized root density and root N concentration. The study also aimed to partition Rs by applying the root regression technique. Rs ranged between 0.06 in December and 1.49 g CO2 m−2 h−1 in August. Average soil temperature alone explained up to 71% of the annual variability of Rs , while soil water content was negatively correlated to Rs . Fertilization, soil C and N concentration and root N had negligible effects on Rs . Fine root density, but not mediumand large-sized root density, contributed to explaining part of the yearly variability of Rs and proved to be a good predictor in December, when the statistical significance of the regression made it possible to estimate the autotrophic component of Rs as being about 3% of total soil respiration.

Several authors (e.g. Lopushinsky and Max (1990), Kuhns et al. (1985)) investigated the influence of soil temperature on the growth of roots of trees. Lopushinsky and Max (1990) found that root growth in seedling transplants of Douglas-fir (Pseudotsuga menziesii (Mirb.) Franco), Pacific silver fir (Abies amabilis(Dougl.) Forbes), noble fir (Abies procera Rehd.), lodgepole pine (Pinus contorta Dougl. ex Loud.) and ponderosa pine (Pines ponderosa Doug. ex Laws.) began when soil temperature exceeded 5 o C. Root growth increased rapidly after 10 o C and attained maximum values at 20 o C. At 30 o C, no root growth occurred in the firs; in the pines, root growth was 30 to 39% of maximum. Maximum shoot growth also occurred at 20 o C. In ponderosa pine, height growth of seedlings from a high-elevation source was unaffected by cold soil, but in low-elevation seedlings it was reduced. Budburst in Douglas-fir and the pines was delayed up to 11 days by cold soil, whereas in silver fir and noble fir, it was only slightly delayed. Prior to new root growth in ponderosa pine, xylem pressure potentials and stomatal conductances during the afternoon indicated reduced stomatal opening at all soil temperatures, whereas 23 days later, stomata were open to a greater degree when temperatures exceeded 10 o C. Kuhns et al.

(1985) evaluated the effects of soil temperature, soil water potential, and leaf water potential on root length growth, number of growing roots, and suberization for three mature black walnut (Juglans nigra L.) trees in an oak-hickory forest in central Missouri. Rhizotrons were used to access the root systems. When only roots growing in wet soils were included, growth began at a soil temperature of 4°C and increased slowly to 13o C, with a more rapid increase above that. Growth rate peaked at 17o to 19o C and the number of growing roots peaked at 21o C, the highest temperature observed. When roots in dry soil were the only ones included in the analysis, root growth was low with a peak at 17o C. Root growth and number of growing roots decreased sharply as soil water potential decreased from 0 to -0.5 MPa, and approached zero as soil water potential went from -0.5 to -1.0 MPa. At low and high soil temperatures suberization rate was high, and at intermediate temperatures it was low. Suberization rate was low at high water potentials and increased as the soil dried. Effects of climate warming on ecosystem productivity are strongly influenced by those on mineralization and uptake of key soil nutrients, particularly N. Models used to project these effects must therefore include a comprehensive and fully coupled N cycle which has undergone 6

rigorous testing. Grant (2014) mentions thay key hypotheses governing the response of the N cycle to warming in the terrestrial ecosystem model ecosys were tested against changes in ecosystem C and N stocks measured during 7 years of 5o C soil heating in the Harvard soil heating experiment. These hypotheses enabled the model to simulate gains in plant C stocks that rose from 50 to 200 g C m−2 y−1 driven by increased N mineralization and uptake as the soil heating experiment progressed. However these gains were offset by continuing losses of soil C stocks from 125 to 250 g C m−2 y−1 driven by increased heterotrophic respiration, so that total C stocks changed little with soil heating. Both gains and losses in the model were consistent with those measured in the soil heating experiment. The changes in N cycling with soil heating on which these model results were based were further corroborated by comparing modeled vs. measured increases in soil N mineralization rates, foliar N contents and reductions in root phytomass, and by comparing modeled increases in CO2 fluxes and net primary productivity with those reported in meta-analyses of warming effects on ecosystem productivity. However when the model was run under gradual climate warming by 5o C per century, these modeled changes in N cycling drove gains in ecosystem C stocks that rose gradually to ca.

165 g C m−2 y−1 after 100 years. The greater gain in ecosystem C modeled under gradual climate warming vs. sudden soil heating was attributed to much smaller losses in soil C stocks. As a conclusion, it may be seen that changes in soil temperature interact with changes in other essential resources. For example, both water and nutrient availability often covary with changes in soil temperature. Higher soil temperatures result in increased nitrogen (N) mineralization if soil waterpotential does not limit microbial activity, see e.g. Pregitzer et al. (2000). Most types of trees can adapt to changing temperatures. Only when the higher temperature is accompanied by a shortage on soil moisture, severe damage may occur, see e.g. Teskey et al. (2015).

References Ceccon, C., Panzacchi, P., Scandellari, F., Prandi, L., Ventura, M., Russo, B., Millard, P., Tagliavini, M., 2011. Spatial and temporal effects of soil temperature and moisture and the relation to fine root density on root and soil respiration in a mature apple orchard. Plant and Soil 342, 195–206. doi:10.1007/s11104-010-0684-8. Chung, H., Muraoka, H., Nakamura, M., Han, S., Muller, O., Son, Y., 2013. Experimental warming studies on tree species and forest ecosystems: a literature review. Journal of Plant Research 126, 447–460. URL: https://doi.org/10.1007/s10265-013-0565-3, doi:10.1007/s10265-013-0565-3. Domisch, T., Finér, L., Lehto, T., 2001. Effects of soil temperature on biomass and carbohydrate allocation in Scots pine (Pinus sylvestris) seedlings at the beginning of the growing season. Tree Physiology 21, 465–472. URL: https://doi.org/10.1093/treephys/21.7.465, doi:10.1093/treephys/21.7.465. Farnsworth, E.J., Nunez-Farfan, J., Careaga, S.A., Bazzaz, F.A., 1995. Phenology and growth of three temperate forest life forms in response to artificial soil warming. Journal of Ecology 83, 967–977. URL: http://www.jstor.org/stable/2261178. Grant, R., 2014. Nitrogen mineralization drives the response of forest productivity to soil

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warming: Modelling in ecosys vs. measurements from the harvard soil heating experiment. Ecological Modelling 288, 38–46. doi:https://doi.org/10.1016/j.ecolmodel.2014.05.015. Hanson, P.J., Riggs, J.S., Nettles, W.R., Phillips, J.R., Krassovski, M.B., Hook, L.A., Gu, L., Richardson, A.D., Aubrecht, D.M., Ricciuto, D.M., Warren, J.M., Barbier, C., 2017. Attaining whole-ecosystem warming using air and deep-soil heating methods with an elevated co2 atmosphere. Biogeosciences 14, 861–883. doi:10.5194/bg-14-861-2017.

Heninger, R.L., White, D.P., 1974. Tree seedling growth at different soil temperatures. Forest Science 20, 363–367. URL: https://doi.org/10.1093/forestscience/20.4.363, doi:10.1093/forestscience/20.4.363, arXiv:https://academic.oup.com/forestscience/article-pdf/20/4/363/23060746/forestscien Kadoya, K., 1978. Studies on the hydrophysiological rhythms of citrus trees. Journal of the Japanese Society for Horticultural Science 47, 167–171. doi:10.2503/jjshs.47.167. Kuhns, M.R., Garrett, H.E., Teskey, R.O., Hinckley, T.M., 1985. Root Growth of Black Walnut Trees Related to Soil Temperature, Soil Water Potential, and Leaf Water Potential. Forest Science 31, 617–629. doi:10.1093/forestscience/31.3.617. Kuiper, P., 1964. Water uptake of higher plants as affected by root temperature. Meded. Landbouwhogeschool Wageningen 64-4 , 11 pp. Lopushinsky, W., Max, T., 1990. Effect of soil temperature on root and shoot growth and on budburst timing in conifer seedling transplants. New Forests 4, 107–124. doi:10.1007/BF00119004. Melissa R.A. Pingree, L.N.K., 2019. The myth of the biological threshold: A review of biological responses to soil heating associated with wildland fire. Forest Ecology and Management 432, 1022–1029. doi:10.1016/j.foreco.2018.10.032. Pausas, J., Llovet, J., Rodrigo, A., Vallejo, R., 2008. Are wildfires a disaster in the mediterranean basin? a review. Int. J.

Wildland Fire 17, 713–723. URL: https://doi.org/10.1071/WF07151. Peng, Y.Y., Dang, Q.L., 2003. Effects of soil temperature on biomass production and allocation in seedlings of four boreal tree species. Forest Ecology and Management 180, 1–9. doi:https://doi.org/10.1016/S0378-1127(02)00486-3. Pregitzer, K.S., King, J., Burton, A., Brown, S., 2000. Responses of tree fine roots to temperature. New Phytologist 147, 105–115. doi:https://doi.org/10.1046/j.1469-8137.2000.00689.x. Teskey, R., Wertin, T., Bauweraerts, I., Ameye, M., McGuire, M., Steppe, K., 2015. Responses of tree species to heat waves and extreme heat events. Plant, Cell & Environment 38, 1699–1712. doi:https://doi.org/10.1111/pce.12417.

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