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Abstract—This paper tracks the annual dynamics of carbon dioxide production (emission and profile concen- tration) by soils of the arboretum in the Moscow ...
ISSN 0147-6874, Moscow University Soil Science Bulletin, 2016, Vol. 71, No. 2, pp. 43–50. © Allerton Press, Inc., 2016. Original Russian Text © O.Yu. Goncharova, O.V. Semenyuk, G.V. Matyshak, A.A. Bobrik, 2016, published in Vestnik Moskovskogo Universiteta. Pochvovedenie, 2016, No. 2, pp. 3–10.

Seasonal Dynamics of Soil CO2 Production in the Arboretum of the Moscow State University Botanical Garden O. Yu. Goncharova, O. V. Semenyuk, G. V. Matyshak, and A. A. Bobrik Department of Soil Science, Moscow State University, Moscow, 119991 Russia e-mail: [email protected], [email protected], [email protected], [email protected] Received May 6, 2016

Abstract—This paper tracks the annual dynamics of carbon dioxide production (emission and profile concentration) by soils of the arboretum in the Moscow State University Botanical Garden that are planted with Siberian spruce and common pine. The high biological activity of the studied soils is caused by the high content of organic matter, slightly alkaline reaction, and good structure and texture. Differences in CO2 production by the soils of a spruce and pine forest (1.5–2 times higher in the latter) can be explained by different structures of soil profiles rather than a temperature regime. The seasonal dynamics of CO2 production are the same for both soils and associated with seasonal changes in climatic parameters. In the cold season, there is noticeable production of carbon dioxide by soils. Keywords: soil temperature regime, CO2 efflux, soil CO2 concentration, Botanical Garden, anthropogenic soils DOI: 10.3103/S0147687416020022

INTRODUCTION In today’s world, there are about 2300 botanical gardens and arboreta, which are centers of floristic and geobotanical studies and educational work in the field of environmental education of the population [2]. At present, there are 99 functioning botanical gardens in Russia, most of which belong to institutions of higher education (universities and agricultural, forestry, and medical institutions). They are the basis for the educational process and implementation of experimental scientific research [9]. Urban botanical gardens should be considered unique artificial ecosystems in which the effect of the urban environment is partially compensated for and a high level of biodiversity is created thanks to the constant investment of resources [8]. An essential attribute of these artificial ecosystems is soil. The soils of the Moscow State University (MSU) Botanical Garden differ from other urban soils, including soils of parks and suburban soils of Moscow oblast. The distinctions are manifested in the structure of the soil profile, chemical properties, and composition of soil biota [6, 7, 12]. The soils of the MSU Botanical Garden have a high fertility level and are relatively weakly polluted. The soil cover is very diverse and includes soils varying from anthropogenically transformed to constructed soils. The soils are an integral component of the unique artificial garden system, and they can be considered the most important environmental object of the study for identification of

similarities with and differences from natural zonal soils and soils of other urban areas. The domestic soil science still applies such approaches rarely [25], although the global ecological studies are currently paying close attention to the functions of urban green areas, such as the absorption and emission of greenhouse gases and carbon sequestration [13–15, 17–19, 21, 22, 24, 26, 27]. The goal of the study is to ascertain the properties of the year-round functioning of soils in the arboretum of the MSU Botanical Garden: to assess the temperature soil regime based on microclimatic data, identify the regularities of seasonal dynamics of CO2 production (efflux and concentration), and compare two ecosystems (spruce and pine forests) with respect to the above-mentioned parameters. MATERIALS AND METHODS The MSU Botanical Garden on Vorobevy Hills, which was founded in 1950, is located at a distance of 800 m to the southwest from the edge of the high right bank of the Moscow River. The territory is composed of weakly permeable covering silty clays and loams, which lie on the moraine. The major works on planning the territory and restoring the fertile layer were carried out in 1950–1951. In the first 10–20 years, lowland peat and fertilizers were introduced into the soils [10]. 43

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Temperature 6° 7°





−10

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−20 Pine forest

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Fig. 1. Average annual temperature profiles of the soils.

The objects of studies are soils planted with Siberian spruce (Picea obovata) and common pine (Pinus sylvestris). The spruce undergrowth includes Norway maple (Acer platanoides) and mountain ash (Sorbus aucuparia), and the underwood includes common honeysuckle (Lonicera xylosteum) and common currant (Ribesia vulgare). Ground elder (Aegopodium podagraria) is predominant in the soil cover; touchme-not (Impatiens noli-tangere) and greater celandine (Chelidonium majus) are also encountered. The foliage cover is 65–70%. The pine undergrowth was noted to include Norway maple, and the ground cover was overgrown with thickets of stinging nettle (Urtica dioica); the foliage cover is high (up to 95%). The studies were carried out in two stationary plots located in the spruce and pine plantations from November 2013 to November 2014, as well as in the winter period of 2012/2013. Annual temperature regime studies included the measurement of air temperature at an interval of 4 h at a height of 1.5 m, on the soil surface and at depths of 10, 20, 40, and 60 cm using ThermochroniButtonTM Sum of positive and negative average daily temperatures for the period from November 2013 to October 2014, degrees centigrade Positive Object Air Soil surface 10 cm 20 cm 40 cm 60 cm

pine forest

spruce forest

3130.6 2640.0 2528.0 2529.2 2531.4 2538.1

Negative pine forest

spruce forest

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–93.8

–146.5

2309.2 2485.1 2444.0 2474.3

–36.8 –4.3 0.0 0.0

–71.7 –4.4 0.0 0.0

programmable micro-temperature sensors [11]. The average annual temperatures at all depths, the sum of temperatures above and below 0°, and the sum of temperatures above 10° were estimated to make an analysis. The difference of the average monthly temperatures in the warmest and coldest months at a depth of 20 cm was taken for the annual temperature amplitude (the continentality of climate, according to Dimo [3]). Frost N-factors (sometimes called “winter” factors) were calculated as the ratio of the sum of average daily soil surface temperatures below zero to the sum of negative air temperatures for the same period. The N-factor (the surface temperature index) is one of the methods for parameterization of the surface energy balance [20]. Proper microclimate measurements were average daily indicators of air temperature. Regime observations over carbon dioxide efflux from the soil surface with removed vegetation were performed by the closed chamber method in three replications in each plot [11, 23]. The efflux was measured once a week in transitional seasons (spring and autumn) and two times a week in stable seasons (winter and summer) from 13:00 to 15:00; the efflux after intense rains was measured not earlier than after 2 days. The exposure time was 10–60 min depending on air temperature. The measurement chamber is a stainless steel cylinder (height of 15 cm and diameter of 10 cm) placed into a plastic base, which is installed in the soil to a depth of 2 cm. Dynamic air sampling from the isolated volume of the ground atmosphere takes places immediately after installing the chamber and after 10–60 min. (The chambers have openings closed with rubber stoppers, which are necessary for sampling.) CO2 concentration was measured by a RMTDX6210 potable infrared gas analyzer. To measure carbon dioxide concentration at different depths (10, 20, 40, and 60 cm), sealed tubes with a diameter of 1 cm and perforation in the lower part were placed into the soil [11, 24]. Samples were taken through a rubber stopper. The data were statistically processed using the Statistica v. 6.0 program. RESULTS AND DISCUSSION Morphological characteristics of the soils. Soil profiles were developed on made-up deposits with various thicknesses, which were laid during the formation of the Botanical Garden. Apparently, subsequently, the upper horizons did not experience mechanical or any other human intervention, since the care of plantings involves the regulation of only vegetation in these biogeocenoses. The spruce plantations are characterized by a thin (0.5 cm) destructive litter [1] that consists of lastyear’s debris. The opened soil profile is formed on made-up deposits of medium-loamy and heavyloamy structure. Its upper part is represented by a

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Fig. 2. CO2 efflux from the soil surface in the spruce forest (the solid line) and pine forest (the dotted line) (a) throughout the year and (b) in spring.

well-marked humus-accumulative horizon (10 cm) of lumpy structure. Below, to a depth of 20 cm, there is a transitional humus horizon with a nonuniform humus content. The lower part of the profile mostly has brownish-yellow shades. The soil features a significant compaction throughout the profile (except for the upper horizon). It should be noted that the profile is highly biogenic up to 80 cm, which is diagnosed based on coprolites and worm traces. All horizons contain anthropomorphic and lithomorphic inclusions; carbonate inclusions and carbonaceous particles are prevalent. Effervescence was noted only for carbonate inclusions. The soil was classified as an urbiquasizem [4] or recreazem [12]. The litter of the pine plantations is thin (0.5 cm), represented by last-year’s debris, and belongs to the destructive type. The peculiarity of the soil profile structure is that it is divided into two parts at a depth of 60 cm: the upper part formed by made-up deposits and the lower part represented by buried horizons of natural zonal sod-podzol soil. The upper part has a MOSCOW UNIVERSITY SOIL SCIENCE BULLETIN

medium-loamy structure with a significant amount of various anthropogenic inclusions throughout the stratum, among which there are carbonate inclusions. The surface humus-accumulative horizon (0.5–7(15) cm) has a brownish dark gray color and lumpy-granular structure with “beads” on plant roots and contains coprolites. The underlying layer (down to 60 cm) is also humic; it is heterogeneous, loose, brownish dark gray, and lumpy-granular. This layer contains many (up to 30%) inclusions, which permits it to be identified as urban, and the presence of inclusions such as iron, porcelain fragments, and wood fragments gives reason to describe this layer as cultural. The soil mass of the made-up layer effervesces from a depth of 5 cm, with the exception of some morphons in the lower part. There, they are lighter and more uniform in color, are denser than the total mass of the horizon, and have fewer inclusions. The lower part of the profile is represented by a fragmentarily well-marked transitional medium-loamy hor. BEL and mediumheavy loamy illuvial hor. BT. The soil was classified as

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than for the spruce forest soil. The sum of active temperatures (>10°C) at a depth of 20 cm is 1852°C (136 days) and 1984°C (142 days) in the spruce and pine forest, respectively. The depth of the penetration of active temperatures in both soils is more than 60 cm. The distinctions in heat availability for the soils in the two ecosystems in the warm period may be due to their different thermal and physical properties (thermal conductivity): the total amount heat arriving to the surface is the same for both soils in this period.

y = 23.829x + 39.461 R2 = 0.7316

600 500 400 300 200 100

−5°

0 0°



10°

15° 20° Temperature

Fig. 3. Dependence of CO2 efflux from the soil surface in the spruce forest on soil temperature at a depth of 10 cm.

an urban stratified gray humic stratozem on a buried soil [4] or culturozem [12]. Soil temperature regime. The pine and spruce forests have a similar annual temperature profile. The average annual temperature changes with depth very insignificantly, rising from 7.0°C on the surface to 7.5°C at a depth of 60 cm. The soil of the spruce forest at a depth of 10 cm, where the average annual temperature falls to 6.5°C, is an exception. In general, the soil of the spruce forest is somewhat colder throughout the profile during the year (Fig. 1). The continentality of both soils in the studied year is about 16°C, which characterizes the temperature regime as moderate. In order to estimate the contribution of positive and negative temperatures to the annual balance, their sum at all depths was calculated (table). The heat availability for the pine forest soil in the warm period (i.e., with positive temperatures) is higher at all depths

In the cold period, the sum of negative temperatures in the pine forest soil (in absolute value) is somewhat lower at all depths than in the spruce forest soil, which can be explained as a result of the different thicknesses and times of occurrence of snow cover. The influence of the latter on the soil surface temperature regime can be estimated using the N-factor: it is much lower in the pine forest than in the spruce forest (0.21 and 0.34), which indicates a greater thickness of snow cover in the former and a greater duration of its occurrence. The dates of the formation of snow cover are clearly registered based on the annual course of average daily temperatures of air and soil surface. They coincide in both plots (January 12–14); moreover, snow cover in the pine forest persists for longer for a month, until about the middle of March. The smaller thickness of snow cover and its rapid disappearance in the spruce forest are due to the greater crown density and presence of forest edges, which are better warmed up in spring. Soil freezing in the studied period was limited to the upper 20 cm. At a depth of 10 cm, the soil was in the frozen state (the average daily soil temperature was lower than –0.5°C) for less than 2 months.

Precipitation, mm 35

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Efflux, mg CO2/(m2 h)

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5 5 0

Nov. 26, 2

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Mar. 26, 2014 May 26, 2014 July 26, 2014

Sept. 26, 2014

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Fig. 5. Seasonal dynamics of CO2 content in the soil profiles of the spruce and pine forests at different depths.

Thus, according to Dimo’s system of classification [3], the studied soils can be classed as belonging to the moderately cold subtype in the seasonally freezing type. The main temperature parameters correspond to those typical for the southern taiga subzone of sodpodzolic soils. In its microclimatic characteristics, the spruce forest soil is colder at all depths in the annual cycle due to lesser heat availability in summer and lower temperatures in winter. The distinction in the temperature regimes of these soils is insignificant. CO2 efflux from the soil surface. Carbon dioxide efflux from the soil surface in the spruce and pine forest varied during the year from 0 to 700 and from 0 to 800 mg CO2/(m2/h), respectively (Fig. 2). In winter, close-to-zero values were observed for about 3 weeks (7 weeks in winter 2012–2013), from February 15 to March 5. The efflux rate surpassed 20 mg CO2/(m2/h) MOSCOW UNIVERSITY SOIL SCIENCE BULLETIN

in the rest of the year. Abrupt growth in carbon dioxide efflux started for both soils in early April and peaked in early July. From late July to mid-August, the process slowed down by a factor of 1.5 and 2.5 in the pine and spruce forest, respectively. Another peak was fixed in mid-September in the pine forest; in the spruce forest, it was less pronounced. An abrupt autumn decrease in efflux was observed from September 20 and was due to a sharp drop in air and soil temperature. A significant correlation in the annual cycle of CO2 efflux was noted for the soils of both ecosystems (R2 = 0.9), but the process was more intense throughout the year in the pine forest (by about 1.5–2 times). Despite the annual trends of CO2 efflux from the soil surface being common for both ecosystems, they may be directed differently in some seasons. This is most strongly pronounced in transitional seasons, in particular, in spring (Fig. 2). As noted above, this fact

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Fig. 6. CO2 efflux from the soil surface, air temperature, and thickness of snow cover in the spruce forest in winter 2012–2013.

is due to the different terms of snowmelt and, accordingly, to different rates of warming of upper soil horizons. CO2 efflux in the annual cycle is weakly correlated with air temperature (R2 = 0.5) and is correlated well with soil temperature at depths of 10 and 20 cm (R2 = 0.7) (Fig. 3). The maximum efflux is observed at moderately warm average daily air temperatures (12– 13°C). At maximum summer temperatures, efflux decreases. Obviously, efflux is largely affected in the warmest period of a year by another factor—moisture. This fact is confirmed by data on the annual dynamics of precipitation (Fig. 4): it was found to be absent in July. CO2 concentration in the soil horizons. Analysis of the seasonal dynamics of carbon dioxide content in the spruce forest soil (Fig. 5) indicated that the profile distribution of CO2 content was relatively stable from May to January: the smallest values of its concentration (1600–3000 ppm) were observed in the upper 10-cm layer and gradually grew with depth. At a depth of 60 cm, it is two to four times higher than at a depth of 10 cm, depending on season. In general, CO2 concentration at a depth of up to 40 cm varies from June to November steadily, no more than within 1000 ppm. There are 3 months that clearly stand out in the overall stable picture: February, March, and April. In this period, a strong upsurge in CO2 concentration takes place at all depths with the exception of 60 cm. CO2 concentration at depths of 10 and 20 cm grew by a factor of 4–5 and 2–3, respectively; at a depth of 40 cm, it increased to the maximum, by a factor of 2–6 (taking values of approximately 20 000 ppm in the gas phase, i.e., 2% in volume). We found no correlation between the abrupt upsurges in carbon dioxide concentration in the soil profile and temperature of both air and soil at all depths. In the period of maximum

concentrations, the soil at a depth of 10 cm had slightly negative temperatures, i.e., still was in the frozen state, and at depths of 20 and 40 cm it was stable: from 0.5 to 1°C. At such a low and stable temperature, it is difficult to suspect some upsurge in microbiological activity. The abrupt upsurges in carbon dioxide concentration in the soil profile may coincide with the activation of root respiration, i.e., with the beginning of the growing season in tree vegetation that is due to the threshold values of day length rather than an increase in air temperature. In addition, this is also due to the gas being fixed in the soil profile in the period in which the upper 10-cm layer is still in the frozen state. This is confirmed by our data, according to which the peak values of CO2 concentration in the soil profile fall in the period with the minimum values of efflux from the surface. After thawing of the soil, commencing at the beginning of April, CO2 is actively released with a strong increase in efflux and decrease in the gas concentration in the profile. This period lasts up to the middle of May. We did not observe upsurges in the peak efflux values, although in this period measurements were carried out at least once a week; in the period of active snowmelt, they were made more frequently—once every 3 days. CO2 concentration in the soil of the pine forest is 1.5–2 times higher at all depths in comparison with the spruce forest. The profile distribution of concentration is similar, except for the depth of 20 cm, where it is somewhat lower than at a depth of 10 cm. This may be influenced by the inhomogeneous structure of the upper horizons, which was indicated in describing the soils. The seasonal dynamics of the profile CO2 concentration in the pine forest are similar to those for the spruce forest. Its abrupt growth is observed at all depths (including 60 cm) in February–April with a gradual reduction during the last month.

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The annual cycle was revealed to have a correlation between CO2 concentration and temperature at a depth of 60 cm (R2 = 0.5). It is absent at other depths. The minimal efflux of the gas from the soil surface takes place in by no means the coldest period, but at the end of winter. We believe this to be solely due to the fixation of the gas during the formation of ice crust on the soil surface at the moment when short-term thaws with an insignificant snowmelt begin. This is also confirmed by our observations over CO2 efflux in winter 2012–13 in the spruce forest (Fig. 6). CONCLUSIONS The obtained data indicate the high biological activity of the soils, which is more likely to be typical to those of deciduous forests [5, 11, 16]. Obviously, this is primarily due to the structural peculiarities and properties of the soils: the high humus content, slightly alkaline reaction (according to effervescence), and well-defined structure. The distinctions in CO2 production by the soils of the spruce and pine forests (it is 1.5–2 times higher in the pine forest), which were registered throughout the year according to the data on both CO2 efflux and its concentration in the soil air are due neither to different temperature regimes of the soils (the distinction is insignificant) nor to the character of plant communities. The main cause is the structure of the soil profile and, probably, the composition of organic matter. The presence of the thick, well-structured, and loose organic-mineral urban (cultural) horizon in the soil of the pine forest ensures intense year-round intrasoil production of carbon dioxide. This horizon favors the emergence of nitrophilous vegetation (for example, stinging nettle) with a large aboveground and underground biomass, which is not characteristic of this forest type. Forming a dense aboveground cover, this plant undoubtedly makes contribution to the increased CO2 production in the growing season at the expense of root respiration. Despite the differences in the absolute values of CO2 production by soils of different plantations, it is observed to have the same seasonal dynamics, which are due to the seasonality of climatic parameters and functioning of vegetation and not associated (or weakly associated) with the structural properties of the soil profile and its artificial origin. The seasonal dynamics of CO2 production by the soils of the Botanical Garden are identical to those of zonal forest soils [11]. From our point of view, this fact suggests the possibility of using artificial ecosystems such as the arboretum of the MSU Botanical Garden as objects for studies related to the turnover of carbon and other biophilic elements, making year-round manipulative experiments to assess the contribution of biogeocenosis components (roots, litter, microflora) to the total carbon dioxide production by soils. MOSCOW UNIVERSITY SOIL SCIENCE BULLETIN

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We can conclude that in the cold period there is a noticeable carbon dioxide production by the soils, which is registered based on the large growth in carbon dioxide content in the soil air. The abrupt decrease in efflux in the second half of winter is due solely to physical processes—fixation of the gas owing to the formation of ice crust on the soil surface. To determine carbon dioxide production in winter, balance estimates of its content in the soil profile need to be made. REFERENCES 1. Bogatyrev, L.G., Demin, V.V., Matyshak, G.V., and Sapozhnikova, V.A., Investigation of forest litters: some theoretical aspects, Lesovedenie, 2004, no. 4, pp. 17–29. 2. Demidov, A.S. and Potapova, S.A., The way to solve the strategic problems on botanical gardens in the field of plants biological diversity saving, Mater. Vseross. konf. posvyashchennoi 60-letiyu so dnya obrazovaniya Instituta biologicheskih problem kriolitozony, Sibirskogo Otdeleniya, Rossiiskoi Akademii Nauk “Biologicheskie problemy kriolitozony,” Yakutsk, 30 iyulya–5 avgusta 2012 (Proc. All-Russian Conf. Dedicated to the 60-th Anniversary of Creation the Institute of Biological Problems on Cryolithozone Siberian Branch of Russian Academy of Sciences: “Biological Problems on Cryolithozone”, July 30–August 5, 2012, Yakutsk), Yakutsk, 2012. 3. Dimo, V.N., Teplovoi rezhim pochv SSSR (Thermal Condition of the Soils of Soviet Union), Moscow: Kolos, 1972. 4. Klassifikatsiya i diagnostika pochv Rossii (Classification and Diagnostics of Russian Soils), Shishov, L.L., Tonkonogov, V.D., Lebedeva, I.I., and Gerasimova, M.I., Eds., Smolensk: Oikumena, 2004. 5. Naumov, A.V., Dykhanie pochvy: sostavlyayushchie, ekologicheskie funktsii, geograficheskie zakonomernosti (Soil Respiration: Components, Ecological Functions, Geographical Regularities), Novosibirsk: Sib. Otd., Ross. Akad. Nauk, 2009. 6. Prokofyeva, T.V., Martynenko, I.A., and Ivannikov, F.A., Classification of Moscow soils and parent materials and its possible inclusion in the Classification System of Russian Soils, Eurasian Soil Sci., 2011, vol. 44, no. 5, pp. 561–571. 7. Prokof’eva, T.V. and Rozanova, M.S., Soil’s morphological diagnostics of Moscow State University botanical garden at Leninskie Gory, Tezisy dokladov mezhdunaraodnoi konferentsii “Biodiagnostika v ekologicheskoi otsenke pochv i sopredel’nykh sred” (Proc. Int. Conf. “Biological Diagnostics in Ecological Estimation for Soils and Adjacent Mediums”), Moscow, 2013. 8. Rappoport, A.V., Moscow State University botanical garden is the model for environment ecological monitoring, Mezhd. konf. “Biodiagnostika v ekologicheskoi otsenke pochv i sopredel'nykh sred,” Tezisy dokladov (Proc. Int. Conf. “Biological Diagnostics in Ecological Estimation for Soils and Adjacent Mediums,” Abstracts of Papers), Moscow, 2013. 9. Rappoport, A.V., Lysak, L.V., Marfenina, O.E., et al., Topical soil and ecological investigations in botanical gardens (by the example of Moscow and St. Peters-

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MOSCOW UNIVERSITY SOIL SCIENCE BULLETIN

Translated by L. Solovyova

Vol. 71

No. 2

2016