Isometric scaling to model water transport in conifer tree rings across time and environments.

The hydraulic properties of xylem determine the ability of plants to efficiently and safely provide water to their leaves. These properties are key to understanding plant responses to environmental conditions and evaluating their fate under a rapidly changing climate. However, their assessment is hindered by the challenges of quantifying basic hydraulic components such as bordered pits and tracheids. Here, we use isometric scaling between tracheids and pit morphology to merge partial hydraulic models of the tracheid component and to upscale these properties to the tree-ring level in conifers. Our new model output is first cross-validated with the literature and then applied to cell anatomical measurements from Larix sibirica tree rings formed under harsh conditions in southern Siberia to quantify the intra- and inter-annual variability in hydraulic properties. The model provides a means of assessing how different-sized tracheid components contribute to the hydraulic properties of the ring. Upscaled results indicate that natural inter- and intra-ring anatomical variations have a substantial impact on the tree's hydraulic properties. Our model facilitates the assessment of important xylem functional attributes because it requires only the more accessible measures of cross-sectional tracheid size. This approach, if applied to dated tree rings, provides a novel way to investigate xylem structure-function relationships across time and environmental conditions.

Ecological and conceptual consequences of Arctic pollution.

Although the effect of pollution on forest health and decline received much attention in the 1980s, it has not been considered to explain the 'Divergence Problem' in dendroclimatology; a decoupling of tree growth from rising air temperatures since the 1970s. Here we use physical and biogeochemical measurements of hundreds of living and dead conifers to reconstruct the impact of heavy industrialisation around Norilsk in northern Siberia. Moreover, we develop a forward model with surface irradiance forcing to quantify long-distance effects of anthropogenic emissions on the functioning and productivity of Siberia's taiga. Downwind from the world's most polluted Arctic region, tree mortality rates of up to 100% have destroyed 24,000 km2 boreal forest since the 1960s, coincident with dramatic increases in atmospheric sulphur, copper, and nickel concentrations. In addition to regional ecosystem devastation, we demonstrate how 'Arctic Dimming' can explain the circumpolar 'Divergence Problem', and discuss implications on the terrestrial carbon cycle.

What prevails in climatic response of Pinus sylvestris in-between its range limits in mountains: slope aspect or elevation?

The roles of slope orientation and elevational temperature gradient were investigated for Scots pine (Pinus sylvestris L.) growth in the middle of its growth range, where these factors can significantly modulate microclimate and thus plant growth. We assumed that slope orientation causes more complex and severe effects than elevation because it influences all three main factors of plant growth: light, heat, and moisture. In addition to the total ring width, the earlywood and latewood width and latewood ratio were considered variables that contain information about tree ring growth during the season and wood structure over all tree life span on three sampling sites at different elevations and opposite slopes. Despite the observed dependence of pine growth rate on temperature and solar radiation, the mean latewood ratio is stable and similar between all sampling sites, being presumably defined by the genotype of individual trees. The seasonality of the climatic response of tree growth is bound to spatiotemporal variation of the vegetative season timing due to the elevational temperature lapse and local warming. However, its direction is primarily defined by slope orientation, where southern slope is moisture-limited, even at adjacent sites, and divergent climatic reactions of earlywood (weak moisture-limited in the last decades) and latewood growth (temperature-limited) were revealed on the northern slope.

New Methods in Digital Wood Anatomy: The Use of Pixel-Contrast Densitometry with Example of Angiosperm Shrubs in Southern Siberia.

This methodological study describes the adaptation of a new method in digital wood anatomy, pixel-contrast densitometry, for angiosperm species. The new method was tested on eight species of shrubs and small trees in Southern Siberia, whose wood structure varies from ring-porous to diffuse-porous, with different spatial organizations of vessels. A two-step transformation of wood cross-section photographs by smoothing and Otsu's classification algorithm was proposed to separate images into cell wall areas and empty spaces within (lumen) and between cells. Good synchronicity between measurements within the ring allowed us to create profiles of wood porosity (proportion of empty spaces) describing the growth ring structure and capturing inter-annual differences between rings. For longer-lived species, 14-32-year series from at least ten specimens were measured. Their analysis revealed that maximum (for all wood types), mean, and minimum porosity (for diffuse-porous wood) in the ring have common external signals, mostly independent of ring width, i.e., they can be used as ecological indicators. Further research directions include a comparison of this method with other approaches in densitometry, clarification of sample processing, and the extraction of ecologically meaningful data from wood structures.

Temperature-induced responses of xylem structure of Larix sibirica (Pinaceae) from the Russian Altay.

PREMISE OF THE STUDY: Xylem structure determines the hydraulic and mechanical properties of a stem, and its plasticity is fundamental for maintaining tree performance under changing conditions. Unveiling the mechanism and the range of xylem adjustment is thus necessary to anticipate climate change impacts on vegetation. METHODS: To understand the mechanistic process and the functional impact of xylem responses to warming in a cold-limited environment, we investigated the relationship between temperature and tracheid anatomy along a 312-yr tree-ring chronology of Larix sibirica trees from the Altay Mountains in Russia. KEY RESULTS: Climate-growth analyses indicated that warming favors wider earlywood cell lumen, thicker latewood walls, denser maximum latewood, and wider rings. The temperature signal of the latewood was stronger (r > 0.7) and covered a longer and more stable period (from June to August) than that of earlywood and tree-ring width. Long-term analyses indicated a diverging trend between lumen and cell wall of early- and latewood. CONCLUSIONS: Xylem anatomy appears to respond to warming temperatures. A warmer early-growing season raises water conduction capacity by increasing the number and size of earlywood tracheids. The higher-performing earlywood tracheids promote more carbon fixation of the latewood cells by incrementing the rate of assimilation when summer conditions are favorable for growth. The diverging long-term variation of lumen and cell wall in earlywood vs. latewood suggests that xylem adjustments in latewood increase mechanical integrity and support increasing tree size under the ameliorated growing conditions.

Modeling of the Statistical Distribution of Tracheids in Conifer Rings: Finding Universal Criterion for Earlywood-Latewood Distinction.

The quantitative description of growth rings is yet incomplete, including the functional division into earlywood and latewood. Methods developed to date, such as the Mork criterion for conifers, can be biased and arbitrary depending on species and growth conditions. We proposed the use of modeling of the statistical distribution of tracheids to determine a universal criterion applicable to all conifer species. Thisstudy was based on 50-year anatomical measurements of Pinus sylvestris L., Pinus sibirica Du Tour, and Picea obovata Ledeb. near the upper tree line in the Western Sayan Mountains (South Siberia). Statistical distributions of the cell wall thickness (CWT)-to-radial-diameter (D) ratio and its slope were investigated for raw and standardized data (divided by the mean). The bimodal distribution of the slope for standardized CWT and D was modeled with beta distributions for earlywood and latewood tracheids and a generalized normal distribution for transition wood to account for the gradual shift in cell traits. The modelcan describe with high accuracy the growth ring structure for species characterized by various proportions of latewood, histometric traits, and gradual or abrupt transition. The proportion of two (or three, including transition wood) zones in the modeled distribution is proposed as a desired criterion.

Factors Limiting Radial Growth of Conifers on Their Semiarid Borders across Kazakhstan.

The forests of Central Asia are biodiversity hotspots at risk from rapid climate change, but they are understudied in terms of the climate-growth relationships of trees. This classical dendroclimatic case study was performed for six conifer forest stands near their semiarid boundaries across Kazakhstan: (1-3) Pinus sylvestris L., temperate forest steppes; (4-5) Picea schrenkiana Fisch. & C.A. Mey, foothills, the Western Tien Shan, southeast; (6) Juniperus seravschanica Kom., montane zone, the Western Tien Shan, southern subtropics. Due to large distances, correlations between local tree-ring width (TRW) chronologies are significant only within species (pine, 0.19-0.50; spruce, 0.55). The most stable climatic response is negative correlations of TRW with maximum temperatures of the previous (from -0.37 to -0.50) and current (from -0.17 to -0.44) growing season. The strength of the positive response to annual precipitation (0.10-0.48) and Standardized Precipitation Evapotranspiration Index (0.15-0.49) depends on local aridity. The timeframe of climatic responses shifts to earlier months north-to-south. For years with maximum and minimum TRW, differences in seasonal maximal temperatures (by ~1-3 °C) and precipitation (by ~12-83%) were also found. Heat stress being the primary factor limiting conifer growth across Kazakhstan, we suggest experiments there on heat protection measures in plantations and for urban trees, alongside broadening the coverage of the dendroclimatic net with accents on the impact of habitat conditions and climate-induced long-term growth dynamics.

VS-Cambium-Developer: A New Predictive Model of Cambium Functioning under the Influence of Environmental Factors.

Climate changes influence seasonal tree-ring formation. The result is a specific cell structure dependent on internal processes and external environmental factors. One way to investigate and analyze these relationships is to apply diverse simulation models of tree-ring growth. Here, we have proposed a new version of the VS-Cambium-Developer model (VS-CD model), which simulates the cambial activity process in conifers. The VS-CD model does not require the manual year-to-year calibration of parameters over a long-term cell production reconstruction or forecast. Instead, it estimates cell production and simulates the dynamics of radial cell development within the growing seasons. Thus, a new software based on R programming technology, able to efficiently adapt to the VS model online platform, has been developed. The model was tested on indirect observations of the cambium functioning in Larix sibirica trees from southern Siberia, namely on the measured annual cell production from 1963 to 2011. The VS-CD model proves to simulate cell production accurately. The results highlighted the efficiency of the presented model and contributed to filling the gap in the simulations of cambial activity, which is critical to predicting the potential impacts of changing environmental conditions on tree growth.

Climate impacts on tree-ring stable isotopes across the Northern Hemispheric boreal zone.

Boreal regions are changing rapidly with anthropogenic global warming. In order to assess risks and impacts of this process, it is crucial to put these observed changes into a long-term perspective. Summer air temperature variability can be well reconstructed from conifer tree rings. While the application of stable isotopes can potentially provide complementary climatic information over different seasons. In this study, we developed new triple stable isotope chronologies in tree-ring cellulose (δ13Ctrc, δ18Otrc, δ2Htrc) from a study site in Canada. Additionally, we performed regional aggregated analysis of available stable isotope chronologies from 6 conifers' tree species across high-latitudinal (HL) and - altitudinal (HA) as well as Siberian (SIB) transects of the Northern Hemispheric boreal zone. Our results show that summer air temperature still plays an important role in determining tree-ring isotope variability at 11 out of 24 sites for δ13Ctrc, 6 out of 18 sites for δ18Otrc and 1 out of 6 sites for δ2Htrc. Precipitation, relative humidity and vapor pressure deficit are significantly and consistently recorded in both δ13Ctrc and δ18Otrc along HL. Summer sunshine duration is captured by all isotopes, mainly for HL and HA transects, indicating an indirect link with an increase in air and leaf temperature. A mixed temperature-precipitation signal is preserved in δ13Ctrc and δ18Otrc along SIB transect. The δ2Htrc data obtained for HL-transect provide information not only about growing seasonal moisture and temperature, but also capture autumn, winter and spring sunshine duration signals. We conclude that a combination of triple stable isotopes in tree-ring studies can provide a comprehensive description of climate variability across the boreal forest zone and improve ecohydrological reconstructions.

Modern aridity in the Altai-Sayan mountain range derived from multiple millennial proxies.

Temperature and precipitation changes are crucial for larch trees growing at high-elevation sites covered by permafrost in the Altai-Sayan mountain range (ASMR). To contextualize the amplitude of recent climate fluctuations, we have to look into the past by analyzing millennial paleoclimatic archives recording both temperature and precipitation. We developed annually resolved 1500-year tree-ring cellulose chronologies (δ13Ccell, δ18Ocell), and used these new records to reconstruct the variability in local summer precipitation and air temperature. We combined our new local reconstructions with existing paleoclimatic archives available for the Altai. The data show a strong decreasing trend by ca. 49% in regional summer precipitation, along with a regional summer temperature increase towards the twenty-first century, relative to the preceding 1500 years. Modern dry conditions (1966-2016 CE) in the ASMR are the result of simultaneous summer warming and decreased precipitation. Our new reconstructions also demonstrate that climate change in the ASMR is much stronger compared to the global average.

Forward Modeling Reveals Multidecadal Trends in Cambial Kinetics and Phenology at Treeline.

Significant alterations of cambial activity might be expected due to climate warming, leading to growing season extension and higher growth rates especially in cold-limited forests. However, assessment of climate-change-driven trends in intra-annual wood formation suffers from the lack of direct observations with a timespan exceeding a few years. We used the Vaganov-Shashkin process-based model to: (i) simulate daily resolved numbers of cambial and differentiating cells; and (ii) develop chronologies of the onset and termination of specific phases of cambial phenology during 1961-2017. We also determined the dominant climatic factor limiting cambial activity for each day. To asses intra-annual model validity, we used 8 years of direct xylogenesis monitoring from the treeline region of the Krkonose Mts. (Czechia). The model exhibits high validity in case of spring phenological phases and a seasonal dynamics of tracheid production, but its precision declines for estimates of autumn phenological phases and growing season duration. The simulations reveal an increasing trend in the number of tracheids produced by cambium each year by 0.42 cells/year. Spring phenological phases (onset of cambial cell growth and tracheid enlargement) show significant shifts toward earlier occurrence in the year (for 0.28-0.34 days/year). In addition, there is a significant increase in simulated growth rates during entire growing season associated with the intra-annual redistribution of the dominant climatic controls over cambial activity. Results suggest that higher growth rates at treeline are driven by (i) temperature-stimulated intensification of spring cambial kinetics, and (ii) decoupling of summer growth rates from the limiting effect of low summer temperature due to higher frequency of climatically optimal days. Our results highlight that the cambial kinetics stimulation by increasing spring and summer temperatures and shifting spring phenology determine the recent growth trends of treeline ecosystems. Redistribution of individual climatic factors controlling cambial activity during the growing season questions the temporal stability of climatic signal of cold forest chronologies under ongoing climate change.

Spring arctic oscillation as a trigger of summer drought in Siberian subarctic over the past 1494 years.

Rapid changes in the hydrological and temperature regimes over the past decades at the northern latitudes enhance significantly permafrost degradation accelerating carbon release, increase the frequency of drought events and extensive wildfires. However, the mechanisms and dynamics driving drought events and their influence on Siberian forests are currently the subject of numerous research activities. Newly developed and annually resolved stable carbon and oxygen isotope chronologies of larch tree-ring cellulose (δ13Ccell and δ18Ocell) for the period 516-2009 CE allowed the reconstruction of July precipitation and Arctic Oscillation (AO) in May, respectively. Unprecedented drought events occurred towards twentieth-twenty-first centuries as indicated by the July precipitation reconstruction. Positive AO phases in May were most pronounced during the second part of the first millennium, but also increased in frequency in the modern period of the twentieth-twenty-first centuries. Negative AO phases are associated with cold anomalies and show a remarkable decrease in the nineteenth century caused by a series of major volcanic eruptions. Our findings help explaining the increased frequency of Siberian forest fires over the past decades in Central Siberia consistent with a reduction of summer precipitation, triggered by a positive phase of the Arctic Oscillation in May.

Non-linear Response to Cell Number Revealed and Eliminated From Long-Term Tracheid Measurements of Scots Pine in Southern Siberia.

Dendroclimatic research offers insight into tree growth-climate response as a solution to the forward problem and provides reconstructions of climatic variables as products of the reverse problem. Methodological developments in dendroclimatology have led to the inclusion of a variety of tree growth parameters in this field. Tree-ring traits developed during short time intervals of a growing season can potentially provide a finer temporal scale of both dendroclimatic applications and offer a better understanding of the mechanisms of tree growth reaction to climatic variations. Furthermore, the transition from classical dendroclimatic studies based on a single integral variable (tree-ring width) to the modern multitude of quantitative variables (e.g., wood anatomical structure) adds a lot of complexity, which mainly arises from intrinsic feedbacks between wood traits and muddles seasonality of registered climatic signal. This study utilized life-long wood anatomical measurements of 150- to 280-year-old trees of Pinus sylvestris L. growing in a moisture-sensitive habitat of the forest-steppe of Southern Siberia (Russia) to investigate and eliminate legacy effect from cell production in tracheid traits. Anatomical parameters were calculated to describe the results of the three main subsequent stages of conifer xylem tracheid development, namely, cell number per radial file in the ring, mean and maximum cell radial diameter, and mean and maximum cell-wall thickness. Although tree-ring width was almost directly proportional to cell number, non-linear relationships with cell number were revealed in tracheid measurements. They exhibited a stronger relationship in the areas of narrow rings and stable anatomical structure in wider rings. The exponential models proposed in this study demonstrated these relationships in numerical terms with morphometric meaning. The ratio of anatomical measurements to their modeled values was used to develop long-term anatomical chronologies, which proved to retain information about climatic fluctuations independent of tree-ring width (cell number), despite decreased common signal.

Small fluctuations in cell wall thickness in pine and spruce xylem: Signal from cambium?

In the conifer tree rings, each tracheid goes through three phases of differentiation before becoming an element of the stem water-conducting structure: division, extension, and cell wall thickening. These phases are long-lasting and separated temporally, especially cell wall thickening. Despite the numerous lines of evidence that external conditions affect the rate of growth processes and the final anatomical dimensions during the respective phases of tracheid differentiation, the influence of the environment on anatomical dimensions during the cell division phase (cambial activity) has not yet been experimentally confirmed. In this communication, we provide indirect evidence of such an effect through observations of the small fluctuations in the latewood cell wall thickness of rapidly growing tree rings, which exhibit a high cell production rate (more than 0.4 cells per day on average). Such small fluctuations in the cell wall thickness cannot be driven by variations in external factors during the secondary wall deposition phase, since this phase overlaps for several tens of latewood cells in the rings of fast-growing trees due to its long duration.

Intra-annual variability of anatomical structure and delta(13)C values within tree rings of spruce and pine in alpine, temperate and boreal Europe.

Tree-ring width, wood density, anatomical structure and (13)C/(12)C ratios expressed as delta(13)C-values of whole wood of Picea abies were investigated for trees growing in closed canopy forest stands. Samples were collected from the alpine Renon site in North Italy, the lowland Hainich site in Central Germany and the boreal Flakaliden site in North Sweden. In addition, Pinus cembra was studied at the alpine site and Pinus sylvestris at the boreal site. The density profiles of tree rings were measured using the DENDRO-2003 densitometer, delta(13)C was measured using high-resolution laser-ablation-combustion-gas chromatography-infra-red mass spectrometry and anatomical characteristics of tree rings (tracheid diameter, cell-wall thickness, cell-wall area and cell-lumen area) were measured using an image analyzer. Based on long-term statistics, climatic variables, such as temperature, precipitation, solar radiation and vapor pressure deficit, explained <20% of the variation in tree-ring width and wood density over consecutive years, while 29-58% of the variation in tree-ring width were explained by autocorrelation between tree rings. An intensive study of tree rings between 1999 and 2003 revealed that tree ring width and delta(13)C-values of whole wood were significantly correlated with length of the growing season, net radiation and vapor pressure deficit. The delta(13)C-values were not correlated with precipitation or temperature. A highly significant correlation was also found between delta(13)C of the early wood of one year and the late wood of the previous year, indicating a carry-over effect of the growing conditions of the previous season on current wood production. This latter effect may explain the high autocorrelation of long-term tree-ring statistics. The pattern, however, was complex, showing stepwise decreases as well as stepwise increases in the delta(13)C between late wood and early wood. The results are interpreted in the context of the biochemistry of wood formation and its linkage to storage products. It is clear that the relations between delta(13)C and tree-ring width and climate are multi-factorial in seasonal climates.

Do centennial tree-ring and stable isotope trends of Larix gmelinii (Rupr.) Rupr. indicate increasing water shortage in the Siberian north?

Tree-ring width of Larix gmelinii (Rupr.) Rupr., ratios of stable isotopes of C (delta(13)C) and O (delta(18)O) of whole wood and cellulose chronologies were obtained for the northern part of central Siberia (Tura, Russia) for the period 1864-2006. A strong decrease in the isotope ratios of O and C (after atmospheric delta(13)C corrections) and tree-ring width was observed for the period 1967-2005, while weather station data show a decrease in July precipitation, along with increasing July air temperature and vapor pressure deficit (VPD). Temperature at the end of May and the whole month of June mainly determines tree radial growth and marks the beginning of the vegetation period in this region. A positive correlation between tree-ring width and July precipitation was found for the calibration period 1929-2005. Positive significant correlations between C isotope chronologies and temperatures of June and July were found for whole wood and cellulose and negative relationships with July precipitation. These relationships are strengthened when the likely physiological response of trees to increased CO(2) is taken into account (by applying a recently developed delta(13)C correction). For the O isotope ratios, positive relationships with annual temperature, VPD of July and a negative correlation with annual precipitation were observed. The delta(18)O in tree rings may reflect annual rather than summer temperatures, due to the late melting of the winter snow and its contribution to the tree water supply in summer. We observed a clear change in the isotope and climate trends after the 1960s, resulting in a drastic change in the relationship between C and O isotope ratios from a negative to a positive correlation. According to isotope fractionation models, this indicates reduced stomatal conductance at a relatively constant photosynthetic rate, as a response of trees to water deficit for the last half century in this permafrost region.

Modeled Tracheidograms Disclose Drought Influence on Pinus sylvestris Tree-Rings Structure From Siberian Forest-Steppe.

Wood formation allows trees to adjust in a changing climate. Understanding what determine its adjustment is crucial to evaluate impacts of climatic changes on trees and forests growth. Despite efforts to characterize wood formation, little is known on its impact on the xylem cellular structure. In this study we apply the Vaganov-Shashkin model to generate synthetic tracheidograms and verify its use to investigate the formation of intra-annual density fluctuations (IADF), one of the most frequent climate tree-ring markers in drought-exposed sites. Results indicate that the model can produce realistic tracheidograms, except for narrow rings (<1 mm), when cambial activity stops due to an excess of drought or a lack of growth vigor. These observations suggest that IADFs are caused by a release of drought limitation to cells formation in the first half of the growing season, but that narrow rings are indicators of an even more extreme and persistent water stress. Taking the example of IADFs formation, this study demonstrated that the Vaganov-Shashkin model is a useful tool to study the climatic impact on tree-ring structures. The ability to produce synthetic tracheidogram represents an unavoidable step to link climate to tree growth and xylem functioning under future scenarios.

Trends in recent temperature and radial tree growth spanning 2000 years across northwest Eurasia.

This paper describes variability in trends of annual tree growth at several locations in the high latitudes of Eurasia, providing a wide regional comparison over a 2000-year period. The study focuses on the nature of local and widespread tree-growth responses to recent warming seen in instrumental observations, available in northern regions for periods ranging from decades to a century. Instrumental temperature data demonstrate differences in seasonal scale of Eurasian warming and the complexity and spatial diversity of tree-growing-season trends in recent decades. A set of long tree-ring chronologies provides empirical evidence of association between inter-annual tree growth and local, primarily summer, temperature variability at each location. These data show no evidence of a recent breakdown in this association as has been found at other high-latitude Northern Hemisphere locations. Using Kendall's concordance, we quantify the time-dependent relationship between growth trends of the long chronologies as a group. This provides strong evidence that the extent of recent widespread warming across northwest Eurasia, with respect to 100- to 200-year trends, is unprecedented in the last 2000 years. An equivalent analysis of simulated temperatures using the HadCM3 model fails to show a similar increase in concordance expected as a consequence of anthropogenic forcing.

Climatically induced interannual variability in aboveground production in forest-tundra and northern taiga of central Siberia.

To investigate the variability of primary production of boreal forest ecosystems under the current climatic changes, we compared the dynamics of annual increments and productivity of the main components of plant community (trees, shrubs, mosses) at three sites in the north of Siberia (Russia). Annual radial growth of trees and shrubs was mostly defined by summer temperature regime (positive correlation), but climatic response of woody plants was species specific and depends on local conditions. Dynamics of annual increments of mosses were opposite to tree growth. The difference in climatic response of the different vegetation components of the forest ecosystems indicates that these components seem to be adapted to use climatic conditions during the short and severe northern summer, and decreasing in annual production of one component is usually combined with the increase of other component productivity. Average productivity in the northern forest ecosystems varies from 0.05 to 0.14 t ha(-1) year(-1) for trees, from 0.05 to 0.18 t ha(-1) year(-1) for shrubs and from 0.54 to 0.66 t ha(-1) year(-1) for mosses. Higher values of tree productivity combined with lower annual moss productivity were found in sites in northern taiga in comparison with forest-tundra. Different tendencies in the productivity of the dominant species from each vegetation level (trees, shrubs, mosses) were indicated for the last 10 years studied (1990-1999): while productivity of mosses is increasing, productivity of trees is decreasing, but there is no obvious trend in the productivity of shrubs. Our results show that in the long term, the main contribution to changes in annual biomass productivity in forest-tundra and northern taiga ecosystems under the predicted climatic changes will be determined by living ground cover.