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Ecological Modelling 306 (2015) 46–56

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Ecological Modelling
journal homepage: www.elsevier.com/locate/ecolmodel

Carbon dioxide sequestration model of a vertical greenery system


Michela Marchi ∗ , Riccardo Maria Pulselli, Nadia Marchettini, Federico Maria Pulselli,
Simone Bastianoni
Department of Earth, Environmental and Physical Sciences, Ecodynamics Group, University of Siena, Pian dei Mantellini 44, 53100 Siena, Italy

a r t i c l e i n f o a b s t r a c t

Article history: A dynamic model simulating carbon dioxide (CO2 ) sequestration by plants embedded in a vertical green-
Available online 30 August 2014 ery system (VGS) was developed. The aim of the model was to demonstrate the advantages, in terms of
CO2 sequestration, obtained by installation of large vegetated wall surfaces in urban areas. The ability of
Keywords: various plants, tested separately or in a mixed-species set, to accumulate carbon in different compart-
Carbon stocked in plants ments and moments of their life (plants, compost, soil and microbial biomass in soil) was quantified.
Carbon in compost
The model simulates a series of processes, from planting and growth of herbaceous plants in the VGS to
Carbon in soil
the end of their lives, when compost is produced from green residues and is added to agricultural soil.
Vertical garden
Perennial herbaceous plants
The amount of CO2 removed from the atmosphere is the portion finally stocked in the soil in the form of
Perennial grass microbial biomass.
The plants considered are commonly used in VGS because they are perennial and suitable for hydro-
ponic culture. Typical Mediterranean climate was assumed for the VGS model. The herbaceous species
selected were the perennial grass Zoysia matrella, the succulent Sedum spurium, Mediterranean shrubs
Salvia nemorosa and Rosmarinus officinalis and flowering ornamental plants Geranium sanguineum, Carex
brunnea and Fatsia japonica.
As estimated by the model, the mean yearly CO2 flow absorbed by plant biomass of these species
(expressed in carbon dioxide equivalents, CO2eq ) was 0.44–3.18 kg CO2eq m−2 of vertical garden. Green
residues from plant replacement and trimming/pruning were treated to produce compost and added
to agricultural soil. We estimated that a 98 m2 VGS can capture an average carbon dioxide flow of
13.41–97.03 kg CO2eq per year. The model predicts increasing long-lasting carbon dioxide accumula-
tion in the VGS over time, indicating a feasible solution for climate change mitigation in urban areas.
The model can be adapted to different plant species and different geographical, climatic and biological
conditions.
© 2014 Elsevier B.V. All rights reserved.

1. Introduction from the atmosphere by carbon (C) uptake is an expected benefit


(Shiah and Kim, 2011).
Vertical greenery systems (VGS) are vegetated structures fixed Carbon accumulation in grass and herbaceous plants in urban
to building façades. Plants or grass are embedded in a vertical layer, areas (public and private gardens and green roofs) has been eval-
fed by an automatic watering and fertilizing system (Pulselli et al., uated in many studies through simulation models and direct
2014). VGS offer multiple benefits as innovative components of measurements (e.g., Goudriaan and Ketner, 1984; Moriwaki and
urban design and increase greenery in built environments lacking Kanda, 2004; Li et al., 2010; Nowak and Greenfield, 2010; Dvorak
green areas (Köhler, 2008). Besides esthetic functions, this technol- and Volder, 2012). Goudriaan and Ketner (1984) developed a global
ogy can help improve environmental and human health (e.g., by carbon cycle model considering long-term projections and accu-
heat island mitigation, improved air quality and acoustic damping) mulation of carbon from dead plants (without composting) in soil.
and also protect buildings from environmental stressors such as Moriwaki and Kanda (2004) measured mean hourly CO2 fluxes
sun and acid rain (Beckett et al., 2000; Nicholls, 1977; Oberndorfer in different seasons by the Eddy covariance method, identifying
et al., 2007; Wong et al., 2010). The removal of carbon dioxide (CO2 ) absorption and release of CO2 from urban areas. Li et al. (2010)
studied the effect of green roofs on ambient CO2 concentrations,
measuring carbon absorption velocity and emission rate by plants
∗ Corresponding author. Tel.: +39 0577 232003; fax: +39 0577 232004. using a sealed glass chamber. Nowak and Greenfield (2010) quan-
E-mail address: marchi27@unisi.it (M. Marchi). tified carbon storage and sequestration rates per unit canopy cover

http://dx.doi.org/10.1016/j.ecolmodel.2014.08.013
0304-3800/© 2014 Elsevier B.V. All rights reserved.
M. Marchi et al. / Ecological Modelling 306 (2015) 46–56 47

(including grass) in several U.S. cities, using the Urban Forest outflow processes (residual biomass from plant replacement
Effect (UFORE) model. Dvorak and Volder (2012) proposed various and trimming);
biomass growth indexes for green roofs, comparing species at max- (2) Carbon in green residues to the composting plant (C I Comp) –
imum and minimum air temperatures and precipitation/irrigation. compost production from the residual biomass releases green-
The aim of the present study was to evaluate CO2 sequestra- house gases due to bio-oxidation reactions;
tion and permanent removal of C by a set of herbaceous species (3) Carbon in compost (C Comp) is the carbon taken up in the com-
commonly used in VGS, assuming systematic implementation of post which is returned to agricultural soil (assuming 1 ha of
a series of processes for managing residual biomass. A dynamic agricultural soil);
model was developed to represent these processes, from plant- (4) Carbon in 1 ha of agricultural soil (C Soil) which varies with the
ing and growth of perennial herbaceous plants to the end of their outflow forcing function representing soil respiration;
lives, also considering return of carbon to soil elsewhere after (5) Carbon in 1 ha of agricultural soil microbial biomass (C mb)
composting the green residues. A VGS hypothetically installed on which varies with nourishment and mortality of the microor-
a building façade in a Mediterranean context (central Italy) was ganisms;
assumed as case study. Herbaceous species, such as spontaneous (6) Long-lasting carbon dioxide accumulation in the system
aromatic herbaceous shrubs and drought-resistant and succulent (Acc CO2 ) which varies with carbon dioxide inflow absorbed
plants, were selected because they adapt to the Mediterranean cli- by plants and outflows released by the system, during compost
mate context and soilless hydroponic culture. production and soil respiration.
Other studies analyze parts of the carbon sequestration cycle
(e.g., considering vegetation and soil separately). The present model The state variables 1–5 are expressed in kg carbon and state
takes a holistic view of the system’s compartments (plants, green variable 6 in kg carbon dioxide equivalent (CO2eq , Table 1).
residues, compost, soil and microbial biomass), assessing the final We assumed 1307 kg of herbaceous plants or 1960 kg of peren-
destination of carbon input into the VGS. The model can be used to nial grass Z. matrella (wet weight) embedded in the 98 m2 VGS,
assess carbon uptake by the species selected or modified to evaluate that generate about 100 kg per year of residual biomass. The car-
different species under different management and environmental bon uptake in each compartment (plants, compost, agricultural soil
conditions. and microbial biomass) was estimated over 25 years, the assumed
lifetime of the VGS. Young plants embedded in VGS grow by up to
2. Materials and methods 29% in biomass, i.e., up to the carrying capacity of the garden (see
suggestions based on direct measurements in Durhman and Rowe,
2.1. Model presentation 2007).
The model is calibrated considering that the carbon stocked in
The dynamic model of CO2 accumulation regards herbaceous the vegetation is completely transferred to the composting plant
species planted in a hypothetical 98 m2 VGS located on a south- over 25 years. The carbon concentrated in compost is around 20%
oriented building façade in Siena (central Italy). The model was of plant biomass dry matter, assumed as recommended maximum
developed using STELLA (version 8.1.4) software and represents value (Ministerial Decree 29-4-2010 n.75). The compost is added
the sequence of major processes: CO2 sequestration by growth of to agricultural soil.
plant biomass; harvesting of green residues (i.e., plant replacement For calibration, we used plant growth and mortality rate data
and pruning/trimming) and composting; compost distribution and published in other studies. Biogenic carbon emissions from com-
assimilation into agricultural soil located elsewhere; carbon uptake posting and the carbon rate in the compost produced were chosen
by microbial biomass in that soil. from reasonable values in the literature. The expected equilibrium
The vegetation selected to simulate CO2 sequestration included occurs when, at the end of the simulation, all the plant biomass
six species of perennial herbaceous plants (1. Sedum spurium, 2. embedded in the VGS is transferred to the composting plant and the
Salvia nemorosa, 3. Rosmarinus officinalis, 4. Geranium sanguineum, compost produced contains almost 20% of the dry weight of the veg-
5. Carex brunnea and 6. Fatsia japonica) and one perennial grass etation used. Growth and mortality rates of soil microbial biomass
(Zoysia matrella). S. nemorosa and R. officinalis are spontaneous and soil respiration rate were chosen from the literature to avoid
aromatic herbaceous shrubs of the Mediterranean basin; G. san- excessive accumulation of carbon in the agricultural soil. Applying
guineum and F. japonica are ornamental flowering plants that this approach, all state variables can be expected to reach maxi-
survive in drought habitats (from the Caucasus and southern Japan, mum levels at a certain time in the simulation, following logistic
respectively); C. brunnea, found in most of the world, is popular dynamics.
in horticulture and wild habitat restoration; S. spurium is a suc-
culent plant native to cold and temperate regions of the northern 2.2. Basic values and equations
hemisphere; Z. matrella is a mat-forming perennial grass native to
temperate coastal southeast Asia and northern Australia. All the The plants analyzed in the model have specific biological
perennial herbaceous species are suitable for typical Mediterranean properties, such as percentage water content, dry matter and
climates. carbon dry weight, as well as survival rate in urban residential
Each plant species was tested individually in the dynamic model greenspaces (Table S.1 in the Supplemental material on-line, see for
to assess its real effectiveness for carbon accumulation. The contri- example Kusano, 1901; Stoddard, 1935; Singh and Yadava, 1974;
bution to carbon uptake by the mixed set of perennial herbaceous Teeri et al., 1986; Körner, 1989; Kjellsson, 1991; Michel et al.,
species was also estimated to obtain an average value (each of the 1993; Rejmánková and Rejmánek, 1995; de Kroon et al., 1996;
six species covered 16.33 m2 of the total 98 m2 ). Peñuelas and Estiarte, 1997; Filonow and Dole, 1999; Cuenca and
State variables, processes, forcing functions and variables used Amo-Marco, 2000; Gupta et al., 2002; Sims and Gamon, 2002;
in the model are shown in Fig. 1, while symbols and related units Vendramini et al., 2002; Clary et al., 2004; Malenĉić et al., 2003;
are illustrated in Table 1. Colom et al., 2004; Lindsay and French, 2004; Terashima et al.,
The state variables were: 2004; Wellwood and Cole, 2004; Monterusso et al., 2005; Kim et al.,
2005; Durhman and Rowe, 2007; Lasseigne et al., 2007; Latocha and
(1) Carbon stocked in plants (C pl) which varies according one Batorska, 2007; Li et al., 2008; Wolf and Lundholm, 2008; Getter
inflow forcing function (carbon absorption by plants) and two et al., 2009; Sánchez-Blanco et al., 2009; Patty et al., 2010; Chen
48 M. Marchi et al. / Ecological Modelling 306 (2015) 46–56

Fig. 1. Conceptual diagram of the model.

et al., 2011; Santana et al., 2012; Forde et al., 1976). Table 2 shows in the atmosphere, up to a half saturation constant of 300 ppm
data for the initial value of carbon stocked in plants, trimming and (Jørgensen and Fath, 2011) and that vegetation converts about
mortality rate of vegetation and maximum plant biomass produc- 6% of the solar radiation intercepted into plant biomass (Aikman,
tion of the vertical garden. The trimming rate is expressed by a 1989). The growth rate of plants, expressed by an increasing
graphic function in STELLA that indicates increasing values over graphic function in STELLA, depends on atmospheric CO2 concen-
time. In fact, annual trimming may slowly promote the rate of tration, precipitation, irrigation and the quantity of nutrients in
plant biomass increase (information provided by vertical garden the irrigation water (Table S.2 in Supplemental material on-line;
manufacturers). Singh and Yadava, 1974; Hirose et al., 1989; Vidal et al., 1990;
No carbon was assumed in the composting plant, compost and Newton, 1991; Speiser and Rowell-Rahier, 1991; Jo and McPherson,
agricultural soil at the beginning of our analysis. We also assumed 1995; Peñuelas and Llusià, 1996; van Iersel, 1997; de Kroon et al.,
that the long-lasting carbon dioxide accumulated in the system was 1998; Lloret et al., 1999; Osborne et al., 2000; Getter et al., 2009;
zero kg at the beginning of the simulation. Onipchenko et al., 2009; Olivier et al., 2011; Bretzel et al., 2012;
Radiation, precipitation and air temperature are uncontrolled Yong-Ángel et al., 2012). Logistic growth function introduced a car-
exogenous variables and are expressed as average annual values rying capacity, corresponding to the maximum amount of carbon
obtained from the weather stations in Siena and Sesto Fiorentino contained in the plant biomass of the vertical garden. Irrigation
(Florence, central Italy) in the year 2012 (14.7 MJ m−2 per year, water is 105–181 l per year for the whole vertical garden area.
742.7 mm per year and 15.1 ◦ C, respectively). We also assumed that Nutrients are 1.06–2.06 kg per year for the whole vertical garden
atmospheric concentrations of CO2 (400 ppm in May 2013, Olivier area, depending on plant species (information provided by vertical
et al., 2013) are increasing at about 5 ppm per year (IPCC, 2013). garden manufacturers).
The basic equations applied in the dynamic model are shown in The second phase is breakdown of green residue in a composting
Table 3. plant to produce compost. Compost production is represented by
The model is organized in a series of process phases, namely a first-order equation. The carbon rate in compost produced each
variation in plant biomass, compost production from green year is represented by a graphic function in STELLA (column 2 of
residues, compost distribution to 1 ha of agricultural soil and long- Table S.3 in the Supplemental material on-line; Siena Ambiente,
lasting carbon dioxide accumulation in the whole system. 2010). We introduced a logistic growth function in the compost
The first phase represents the variation in plant biomass due production equation, in which the maximum percentage of carbon
to annual CO2 uptake and carbon loss by trimming and natu- in compost was almost 20% of green residue dry matter. The equa-
ral mortality of vegetation. The influence of solar radiation and tion contained the percentage of C in potential green residue (dry
carbon dioxide concentration on photosynthetic activity are repre- weight basis; C dw) going to the compost plant.
sented by a Michaelis–Menten expression. We assumed that plant The carbon emitted to the atmosphere by biogenic reactions
uptake increased with increasing concentration of carbon dioxide occurring during composting was derived from a range of values
M. Marchi et al. / Ecological Modelling 306 (2015) 46–56 49

Table 1
Summary of the symbols used in the model with descriptions and units.

Symbol Description Unit

State variablesa
Acc CO2 Long-lasting carbon dioxide accumulation in the system kg CO2eq
C Comp Carbon in compost kg C
C I Comp Carbon in green residues to the composting plant kg C
C mb Carbon in 1 ha of soil microbial biomass kg C in 1 ha of agricultural soil
C pl Carbon stocked in plants (above ground and roots) kg C for the whole vertical garden area
C Soil Carbon in 1 ha of agricultural soil (receiving the compost kg C in 1 ha of agricultural soil
produced)

Processes
Comp production Compost production in composting plant kg C per year
Distrib soil Carbon distributed to 1 ha of agricultural soil (using the kg C per year in 1 ha of agricultural soil
compost produced)
Mort mb Mortality of soil microbial biomass kg C per year in 1 ha of agricultural soil
Mort pl Mortality of vegetation in vertical garden kg C per year for the whole vertical garden area
Nutr mb Nutrition of soil microbial biomass kg C per year in 1 ha of agricultural soil
Trim pl Carbon lost by trimmed vegetation kg C per year for the whole vertical garden area

Forcing functions
CH4 emiss CH4 -Cb emissions from compost production kg C per year
CO2 emiss Biogenic carbon emissions from compost production kg C per year
CO2 Release Carbon dioxide flow released by the system kg CO2eq per year
CO2 Uptake pl Carbon dioxide flow absorbed by plants kg CO2 per year for the whole vertical garden area
Resp Soil respiration kg C per year in 1 ha of agricultural soil
Uptake pl Carbon absorption by plants kg C per year for the whole vertical garden area

Variables

Air temp Mean annual air temperature C
C dw Carbon in plants (dry weight) %C dry weight basis
C in Comp Carbon rate in compost kg C per year
C ww Carbon in plants (wet weight) %C wet weight basis
CO2 C pl Carbon dioxide stocked in plants kg CO2 per year for the whole vertical garden area
CO2 Input Output Balance Carbon dioxide flow retained in the system kg CO2eq per year
Concen CO2 A Atmospheric concentration of CO2 ppm CO2 per year
Distrib rate Carbon distribution rate to 1 ha of agricultural soil, using the kg C per year in 1 ha of agricultural soil
produced compost
EF CH4 CH4 emission factor from the composting plant g CH4 per kg biomass(wet weight)
EF CO2 Carbon emission factor (biogenic origin) from the composting g C per kg biomass (wet weight)
plant
factor G Factor regulating photosynthesis, depending on factor1, kg nutrients in water per year for the whole vertical garden area
factor I and factor2
factor I Irrigation factor regulating photosynthesis l per year for the whole vertical garden area
factor1 Precipitation factor regulating photosynthesis mm per year for the whole vertical garden area
factor2 Nutrient factor regulating photosynthesis kg nutrients per year for the whole vertical garden area
Grate mb Growth rate of soil microbial biomass kg C per year in 1 ha of agricultural soil
Grate pl Growth rate of plants kg C per year for the whole vertical garden area
Irrigation Irrigation l per year
Max C Comp Maximum compost production kg C per year
MaxG pl Maximum plant biomass production of the vertical garden kg C per year for the whole vertical garden area
Mrate mb Mortality rate of soil microbial biomass kg C per year in 1 ha of agricultural soil
Mrate pl Mortality rate of plants in vertical garden kg C per year for the whole vertical garden area
Nutrients in water Nutrients in irrigation water kg nutrients per year for the whole vertical garden area
Precipitation Precipitation mm per year for the whole vertical garden area
Rad Mean solar radiation MJ m−2 per year
Trim rate Plant trimming rate kg C per year for the whole vertical garden area
a
The subdivision of state variables, processes, forcing functions and variables is according to the symbols applied to create a conceptual diagram using STELLA (Fig. 1). State
variables are boxes for which differential equations are formulated as accumulation. Processes are thick arrows with a valve symbol between two state variables. Forcing
functions are thick arrows starting or ending as a cloud. Circles are variables in general (Jørgensen, 2009).
b
Carbon in methane (CH4 -C).

between 5.5 and 53.6 g C per kg of green waste (column 3 of Table growth dynamic, adding to the soil the maximum quantity of com-
S.3 in the Supplemental material on-line; see also Michel et al., post produced in a range of 20.56–150.37 kg C per year, depending
1993; Hellebrand, 1998; Komilis and Ham, 2000, 2006; Sommer on plant species (column 5 of Table S.3 in the Supplemental material
and Møller, 2000; ROU, 2001; Weppen, 2001; Komilis, 2006). On the on-line).
other hand, anthropogenic methane (CH4 ) emissions were 0.05 g Nutrition of soil microbial biomass is written as a time-
CH4 per kg of green waste, as proposed by the National Handbook dependent Michaelis–Menten expression, whose constant
of Emission Factors (ANPA CTN-ACE, 2002). (100,000) corresponds to the saturation quantity of carbon in
The third phase represents the carbon stocked in 1 ha of agricul- soil (this value was used in Marchi et al., 2012). The mortality
tural soil and the microbial biomass produced by distributing the rate of soil microbial biomass is very low (expressed by a graphic
compost. Carbon addition to 1 ha of agricultural soil is expressed function in STELLA; column 6 of Table S.3 in the Supplemental
by a first-order equation, in which the compost distribution rate is material on-line) and the growth rate is higher than the mortality
0.23–0.36 kg C per year (column 4 of Table S.3 in the Supplemental rate (0.42 kg C per year in 1 ha of agricultural soil). Soil respiration
material on-line; Siena Ambiente, 2010). We introduced a logistic is characterized by a respiration rate of 0.07 kg C per year and
50 M. Marchi et al. / Ecological Modelling 306 (2015) 46–56

Table 2
Initial value (quantity) of carbon stocked in plants and parameters directly related to vegetation.

Plant species Carbon stocked Plant trimming Mortality of Maximum


in plants ratea vegetation in plant biomass
(initial value)a vertical production of
gardena the vertical
gardena

kg C for the kg C per year kg C per year kg C per year


whole vertical for the whole for the whole for the whole
garden area vertical garden vertical garden vertical garden
area area area

S. spurium 36.6 GRAPH(TIME) 0.1385 47.06


(0.00, 4.759), (1.04, 4.760), (2.08, 4.761), (3.13, 4.762), (4.17, 4.763), (5.21,
4.764), (6.25, 4.765), (7.29, 4.766), (8.33, 4.767), (9.38, 4.768), (10.4, 4.769),
(11.5, 4.77), (12.5, 4.771), (13.5, 4.772), (14.6, 4.773), (15.6, 4.774), (16.7,
4.775), (17.7, 4.776), (18.8, 4.777), (19.8, 4.778), (20.8, 4.779), (21.9, 4.78),
(22.9, 4.781), (24.0, 4.782), (25.0, 4.783)

S. nemorosa 269.89 GRAPH(TIME) 0.2590 347.00


(0.00, 20.649), (1.04, 20.650), (2.08, 20.651), (3.13, 20.652), (4.17, 20.653),
(5.21, 20.654), (6.25, 20.655), (7.29, 20.656), (8.33, 20.657), (9.38, 20.658),
(10.4, 20.659), (11.5, 20.660), (12.5, 20.661), (13.5, 20.662), (14.6, 20.663),
(15.6, 20.664), (16.7, 20.665), (17.7, 20.666), (18.8, 20.667), (19.8, 20.668),
(20.8, 20.669), (21.9, 20.670), (22.9, 20.671), (24.0, 20.672), (25.0, 20.673)

R. officinalis 227.22 GRAPH(TIME) 0.06045 292.13


(0.00, 13.633), (1.04, 13.634), (2.08, 13.635), (3.13, 13.636), (4.17, 13.637),
(5.21, 13.638), (6.25, 13.639), (7.29, 13.640), (8.33, 13.641), (9.38, 13.642),
(10.4, 13.643), (11.5, 13.644), (12.5, 13.645), (13.5, 13.646), (14.6, 13.647),
(15.6, 13.648), (16.7, 13.649), (17.7, 13.650), (18.8, 13.651), (19.8, 13.652),
(20.8, 13.653), (21.9, 13.654), (22.9, 13.655), (24.0, 13.656), (25.0, 13.657)

G. sanguineum 93.19 GRAPH(TIME) 0.1685 119.81


(0.00, 7.130), (1.04, 7.131), (2.08, 7.132), (3.13, 7.133), (4.17, 7.134), (5.21,
7.135), (6.25, 7.136), (7.29, 7.137), (8.33, 7.138), (9.38, 7.139), (10.4, 7.140),
(11.5, 7.141), (12.5, 7.142), (13.5, 7.143), (14.6, 7.144), (15.6, 7.145), (16.7,
7.146), (17.7, 7.147), (18.8, 7.148), (19.8, 7.149), (20.8, 7.150), (21.9, 7.151),
(22.9, 7.152), (24.0, 7.153), (25.0, 7.154)

C. brunnea 231.83 GRAPH(TIME) 0.31645 298.07


(0.00, 17.738), (1.04, 17.739), (2.08, 17.740), (3.13, 17.741), (4.17, 17.742),
(5.21, 17.743), (6.25, 17.744), (7.29, 17.745), (8.33, 17.746), (9.38, 17.747),
(10.4, 17.748), (11.5, 17.749), (12.5, 17.750), (13.5, 17.751), (14.6, 17.752),
(15.6, 17.753), (16.7, 17.754), (17.7, 17.755), (18.8, 17.756), (19.8, 17.757),
(20.8, 17.758), (21.9, 17.759), (22.9, 17.760), (24.0, 17.761), (25.0, 17.762)

F. japonica 116.32 GRAPH(TIME) 0.22 149.56


(0.00, 8.900), (1.04, 8.901), (2.08, 8.902), (3.13, 8.903), (4.17, 8.904), (5.21,
8.905), (6.25, 8.906), (7.29, 8.907), (8.33, 8.908), (9.38, 8.909), (10.4, 8.910),
(11.5, 8.911), (12.5, 8.912), (13.5, 8.913), (14.6, 8.914), (15.6, 8.915), (16.7,
8.916), (17.7, 8.917), (18.8, 8.918), (19.8, 8.919), (20.8, 8.920), (21.9, 8.921),
(22.9, 8.922), (24.0, 8.923), (25.0, 8.924)

Z. matrella 285.38 GRAPH(TIME) 0.17625b 366.91


(0.00, 14.560), (1.04, 14.561), (2.08, 14.562), (3.13, 14.563), (4.17, 14.564),
(5.21, 14.565), (6.25, 14.566), (7.29, 14.567), (8.33, 14.568), (9.38, 14.569),
(10.4, 14.570), (11.5, 14.571), (12.5, 14.572), (13.5, 14.573), (14.6, 14.574),
(15.6, 14.575), (16.7, 14.576), (17.7, 14.577), (18.8, 14.578), (19.8, 14.579),
(20.8, 14.580), (21.9, 14.581), (22.9, 14.582), (24.0, 14.583), (25.0, 14.584)

Mixed-perennial 160.6 GRAPH(TIME) 0.1856 206.49


herbaceous (0.00, 12.288), (1.04, 12.289), (2.08, 12.290), (3.13, 12.291), (4.17, 12.292),
species setc (5.21, 12.293), (6.25, 12.294), (7.29, 12.295), (8.33, 12.296), (9.38, 12.297),
(10.4, 12.298), (11.5, 12.299), (12.5, 12.300), (13.5, 12.301), (14.6, 12.302),
(15.6, 12.303), (16.7, 12.304), (17.7, 12.305), (18.8, 12.306), (19.8, 12.307),
(20.8, 12.308), (21.9, 12.309), (22.9, 12.310), (24.0, 12.311), (25.0, 12.312)
a
The present carbon quantity were calculated from the percentages shown in Table S.1 in the Supplemental material on-line.
b
The mortality rate of Z. matrella was 10.13% of the total of all plants in the vertical garden. We added another 5.1% to this value due to removal of live grass in the same
felt pad in which grass died (15.2%). The grassy felt pad must be totally replaced.
c
Values obtained averaging literature data for S. spurium, S. nemorosa, R. officinalis, G. sanguineum, C. brunnea, F. japonica (Table S.1 in the Supplemental material on-line).

a constant (30,000) that represents soil degradation (a similar the values obtained by the Global Warming Potentials1 (GWP; IPCC,
parameter was used in Jørgensen and Nielsen, 2015). We used 2007).
the parameter values and equations representing nutrition and
mortality of microbial biomass, as well as soil respiration, reported
in Marchi et al. (2012) and Schlesinger (1984).
1
Temperature functions are calculated by an Arrhenius equation. Global Warming Potential (GWP) is an index that represents the relative long-
term contribution of a gas to global warming, compared to another (the reference
Carbon is converted into carbon dioxide equivalents (CO2eq ) on
gas is CO2 ). This index is weighted for the atmospheric residence time of the gas and
the basis of the molecular weights of C, CO2 and CH4 , multiplying its capacity to absorb infrared radiation emitted by the Earth.
M. Marchi et al. / Ecological Modelling 306 (2015) 46–56 51

Table 3
Basic equations used in the model.

First phase: variation in plant biomass


C pl(t) = C pl(t-dt) + (Uptake pl-Mort pl-Harvesting pl) * dt
Concen CO2 A = 400 + (5 * TIME)
factor G = factor1 * factor I * factor2
factor I = IF(Irrigation) < 100a THEN(Irrigation/100a )ELSE (1)
factor1 = IF(Precipitation) < 500 THEN(Precipitation/500)ELSE (1)
factor2 = IF(Nutrients in water) < 1.05b THEN(Nutrients in water/1.05b )ELSE (1)
Grate pl = GRAPH(TIME * factor G)
Mort pl = (Mrate pl * (1.05ˆ(Air temp-20))) * C pl
Trim pl = Trim rate
Uptake pl = (Concen CO2 A/(Concen CO2 A + 300)) * (Rad/(Rad + 6)) * (1.05ˆ(Air temp-20)) * Grate pl * C pl * (1 − (C pl/MaxG pl))

Second phase: compost production from green residues


C I Comp(t) = C I Comp(t-dt) + (Mort pl + Harvesting pl-CO2 emiss-CH4 emiss-Comp production) * dt
CH4 emiss = (((C I Comp * 100/C wwc ) * EF CH4 )/1000) * 12.0107/16.04246
CO2 emiss = ((C I Comp * 100/C wwc ) * EF CO2 )/1000
Comp production = C I Comp * C in Comp * (1 − (C Comp/((C pl * 100/C dw) * 20/100)))

Third phase: carbon accumulation in 1 ha of agricultural soil


C Comp(t) = C Comp(t-dt) + (Comp production-Distrib soil) * dt
C mb(t) = C mb(t-dt) + (Nutr mb-Mort mb) * dt
C Soil(t) = C Soil(t-dt) + (Distrib soil + Mort mb-Nutr mb-Resp) * dt
Distrib soil = C comp * Distrib rate * (1 − (C Soil/Max C Comp))
Grate mb = 0.42 * (factor 1 * (1.05ˆ(Air temp-20)))
Mort mb = (Mrate mb * (1.05ˆ(Air temp-20)) * C mb)
Nutr mb = Grate mb * C mb * (1.05ˆ(Air temp-20)) * (C Soil/(C Soil + 100,000))
Resp = (C Soil * C mb * (1.05ˆ(Air temp-20)) * 0.07)/30,000

Fourth phase: Long-lasting carbon dioxide accumulation in the system


Acc CO2 (t) = Acc CO2(t-dt) + (CO2 Uptake pl-CO2 Release) * dt
CO2 C pl = C pl * 44.0095/12.0107
CO2 In Output Balance = (Uptake pl * 44.0095/12.0107) − (((Resp + CO2 emiss) * 44.0095/12.0107) + ((CH4 emiss * 16.04246/12.0107) * 25))
CO2 Release = (((Resp + CO2 emiss) * 44.0095/12.0107) + ((CH4 emiss * 16.04246/12.0107) * 25))
CO2 Uptake pl = Uptake pl * 44.0095/12.0107
a
100 l water per year is substituted by 176 l water per year, depending on species (other herbaceous plants or grass, respectively).
b
1.05 kg Nutrients per year is substituted by 2.05 kg nutrients per year, depending on species (other herbaceous plants or grass, respectively).
c
We used percentage of carbon in plant biomass, wet weight basis (C ww), since the emission factors are expressed per kg of green plants (wet weight).

The fourth phase represents long-lasting carbon dioxide accu- Fig. 2 shows the stock of carbon in plants, green residues, com-
mulation in the whole system. Carbon dioxide flow retained in post, 1 ha of agricultural soil and microbial biomass (state variables)
the system (CO2 Input Output Balance) is calculated subtracting over 25 years of simulation. In this case, the mixed-perennial herba-
soil respiration and CO2eq emissions due to compost production ceous species set was considered.
from carbon dioxide uptake by plants. An elevated value indicates The average annual carbon concentration was 189.73 kg in veg-
that CO2eq uptake by plant tissue is higher than the losses of the etation, 131.51 kg in the composting plant, 55.03 kg in compost,
whole system, suggesting low carbon inputs to compost, soil and 51.05 kg in 1 ha of agricultural soil and 1550.97 kg in microbial
microbial biomass. Long-lasting carbon dioxide accumulation in biomass. Maximum values of all state variables were reached after
the system (Acc CO2 ) is expressed by a differential equation, for- about 20 years in the simulation.
mulated as accumulation resulting from plant uptake inflow and Long-lasting carbon dioxide accumulation in all compartments,
CO2eq release outflows due to agricultural soil respiration and bio- carbon dioxide flow absorbed by plant tissues, and that released or
oxidation of green residues in the composting facility. retained in the system by the mixed-perennial herbaceous species
set are reported in Fig. 3.
Average annual flows were: 154.25 kg CO2eq for uptake by
3. Results plants, 93.38 kg CO2eq for emissions and 60.87 kg CO2eq for carbon
dioxide retained in the system. Average annual long-lasting carbon
The carbon stocked in the state variables (stocks) as well as the dioxide accumulation in all compartments was 975.34 kg CO2eq and
CO2eq flow balance of the whole system are shown in Table 4 for showed an increasing trend over time.
each plant species. Considering all the simulations (separate species or mixed-plant
The carbon stocks represented by the state variables differed in set), the best species at actively accumulating carbon dioxide in its
the various plant species. Z. matrella stocked the greatest amount tissues was C. brunnea, whereas R. officinalis retained the greatest
of carbon in its tissues, whereas S. nemorosa made a high con- carbon dioxide flow in the system. On the other hand, S. nemorosa
tribution to carbon stocked in compost. Differences in stocked was the best at accumulating carbon dioxide in all compartments
carbon between compartments showed a decreasing trend from in the long period.
one compartment to the next. We estimated that a 98 m2 VGS
can retain a carbon dioxide flow of 13.41–97.03 kg CO2eq per year 4. Discussion
in the system. In particular, it ranges from 0.14 (S. spurium) to
0.99 kg CO2eq m−2 (R. officinalis) of vertical garden per year. On the Carbon accumulating in vegetation represents plant biomass
other hand, S. nemorosa was responsible for 1640.27 kg CO2eq of increase over time. It plays a very important role in this model;
long-lasting carbon dioxide accumulation in the system. This was indeed, the other carbon stocks are estimated from it. The carbon
the highest carbon dioxide sequestration, followed by those of Z. stocked in plants of each species (as biomass variation per square
matrella (1504.63 kg CO2eq ) and R. officinalis (1226.14 kg CO2eq ). meter in the first two years of simulation) according to the model
52 M. Marchi et al. / Ecological Modelling 306 (2015) 46–56

Table 4
Carbon stocked in the state variables, and CO2eq absorption, release and sequestration for each plant species.

State variables Unit S. spurium S. nemorosa R. officinalis G. sanguineum C. brunnea F. japonica Z. matrella
(STOCKS)

Carbon stocked in Average kg C per year for the 43.52 297.47 284.74 105.22 260.12 130.14 312.03
plants (above ground whole vertical garden area
and roots)a kg C for the whole vertical 44.71 312.33 288.46 109.81 271.58 136.09 320.19
garden after 25 years

Carbon in green Average kg C per year 30.40 218.06 154.98 72.24 201.47 94.21 206.15
residues to the kg C after 25 years 44.71 312.33 288.46 109.81 271.58 136.09 320.19
composting plantb
Carbon in compostb Average kg C per year 13.29 104.69 64.66 30.18 82.65 39.33 94.04
kg C after 25 years 20.56 132.62 114.88 46.93 122.50 60.11 150.37

Carbon in 1 ha of Average kg C per year in 1 ha 12.36 97.42 58.14 27.91 76.48 36.30 86.10
agricultural soil agricultural soil
(adding the compost kg C in 1 ha agricultural soil 20.04 130.98 108.58 45.79 199.84 28.71 145.58
produced)b after 25 years

Carbon in 1 ha of Average kg C per year in 1 ha 1550.30 1553.13 1551.00 1550.30 1551.81 1550.49 1552.03
agricultural soil agricultural soil
microbial biomassc kg C in 1 ha agricultural soil 1550.74 1556.80 1552.63 1550.68 1554.01 1551.04 1554.89
after 25 years

Long-lasting carbon Average kg CO2eq per year in 219.27 1640.27 1226.14 511.26 1417.95 662.50 1504.63
dioxide accumulation the system
in the systemb kg CO2eq in the system after 25 314.42 2260.96 2084.94 776.98 2011.39 980.48 2363.40
years

Forcing functions (FLOWS)


Carbon dioxide flow Average kg CO2eq per year for 36.75d 304.65d 122.56d 80.10d 309.59d 118.54d 218.22d
absorbed by plants the whole vertical garden area
kg CO2eq for the whole vertical 35.57 311.84 100.63 80.38 315.06 120.13 217.92
garden area after 25 years

Carbon dioxide flow Average kg CO2eq per year 23.34 211.99 25.53 48.40 225.70 78.34 122.05
released by the system kg CO2eq after 25 years 34.23 302.53 47.25 73.33 303.42 112.82 188.91

Variable (FLOW)
Carbon dioxide flow Average kg CO2eq per year 13.41 92.66 97.03 31.70 83.89 40.20 96.17
retained in the system kg CO2eq after 25 years 1.34 9.31 53.37 7.05 11.64 7.31 29.01
a
The initial values of carbon stocked in plants are reported in Table 2.
b
The initial values of carbon in green residues to the composting plant, in compost and in 1 ha of agricultural soil, as well as the long-lasting carbon dioxide accumulation
in the system, were 0 kg (see Section 2).
c
We considered an initial value of 1550 kg C in soil microbial biomass, on the basis of data on microorganisms in 1 ha of agricultural soil (e.g., Sainju et al., 2003 and Marchi
et al., 2012). The carbon stock in this state variable is high due to the elevated initial value.
d
Average annual active CO2 uptake by plants per square meter of vertical garden was 0.44 kg CO2eq m−2 for S. spurium, 3.04 kg CO2eq m−2 for S. nemorosa, 2.91 kg CO2eq m−2
for R. officinalis, 1.07 kg CO2eq m−2 for G. sanguineum, 2.65 kg CO2eq m−2 for C. brunnea, 1.33 kg CO2eq m−2 for F. japonica and 3.18 kg CO2eq m−2 for Z. matrella.

Fig. 2. Carbon stocked in the state variables for the mixed-perennial herbaceous species set. C pl (Carbon stocked in plants), C I Comp (Carbon in green residues to the
composting plant), C Comp (Carbon in compost), S Soil (Carbon in 1 ha of agricultural soil), C mb (Carbon in 1 ha of agricultural soil microbial biomass).
M. Marchi et al. / Ecological Modelling 306 (2015) 46–56 53

Fig. 3. CO2eq flow absorbed by plants, released and retained in the system for the mixed-perennial herbaceous species set. CO2 Uptake pl (Carbon dioxide flow absorbed by
plants), CO2 Release (Carbon dioxide flow released by the system), CO2 Input Output Balance (Carbon dioxide flow retained in the system), Acc CO2 (Long-lasting carbon
dioxide accumulation in the system).

Table 5
Comparison of the carbon sequestration per square meter obtained with the model after one year of simulation and annual uptake data from the literature.

Plant species Model References

Carbon stocked in plants Carbon stocked in plants (variation in two years)


(variation in the first two years
of simulationa )

kg C m−2 kg C m−2 Source of data

S. spurium 0.0513 0.0528 (±0.0188) Getter et al. (2009)


S. nemorosa 0.0639 0.0781 (±0.0147) van Iersel (1997), Bretzel et al. (2012)
R. officinalis 0.5748 0.4970 (±0.1740) Osborne et al. (2000)
G. sanguineum 0.0440 0.0392 (±0.0070) Onipchenko et al. (2009)
C. brunnea 0.1161 0.0963 (±0.0199) Hirose et al. (1989)
F. japonica 0.0465 0.0439 (±0.0104) Araus et al. (1986)
Z. matrella 0.1230 0.1106 (±0.0201) Jo and McPherson (1995)
a
Variations in carbon stocked in plants (first and second year of simulation). We considered the variation in carbon stock in the first two years of simulation because we
assumed that young plants would grow fast.

was compared with the biomass variation proposed by previous dry matter percentage and natural mortality of plants. In fact,
studies in Table 5. in the case of high carbon percentage (dry weight basis), the
The literature data in Table 5 was obtained by direct measure- model indicates a high capacity to accumulate carbon in plant
ments of biomass variation. The values obtained by the dynamic tissues. Perennial grass Z. matrella has the same water content
model are in line with those drawn from the literature, falling and dry matter percentage as R. officinalis, but the latter has a
within the standard deviations proposed in the references. This pro- higher carbon percentage (dry weight basis) (see Table 2 and
vides a first level validation of the model results. We could not apply Table S.1 in on-line Supplemental material). Z. matrella there-
site-specific measured data because the VGS is only a virtual pro- fore accumulates more carbon in its tissues than R. officinalis,
totype. We therefore used literature data to estimate and validate and showed the highest values of CO2 storage in plant biomass
the carbon stocked in plants. The direct measurements obtained and the highest plant production in the VGS (Table 4). The aro-
from other published experiments (3rd column of Table 5) were matic shrub R. officinalis is a component of Mediterranean maquis
used to partially validate the carbon stocked in plants estimated by and has quite a high water content in leaves and stems. Thus,
the model, converting the literature values into kg C m−2 as a unit of S. nemorosa stocks more carbon in its tissues than R. officinalis,
comparison; e.g., 220.83 g dry matter of C. brunnea per square meter in line with various studies (e.g., Gratani and Varone, 2004). The
(directly measured by Hirose et al., 1989) was divided by 1000 species with the lowest ability to accumulate carbon in tissues
and multiplied by 43.6/100 (representing the percentage of carbon, was S. spurium, because, as a succulent, its dry matter percent-
dry weight basis) to obtain the corresponding value in kg C m−2 . age is very low (Table 2 and Table S.1 in Supplemental material
The other literature figures, including standard deviations, were on-line).
obtained using the same criteria. A major role in the variation of carbon stocked in different
Carbon sequestration in plant tissues mainly depends on the plants is also played by their specific growth and mortality rate (see
biological properties of the species: for example, water content, Tables S.1 and S.2 in the Supplemental material on-line). The carbon
54 M. Marchi et al. / Ecological Modelling 306 (2015) 46–56

stocked in plants increases over the years, approaching maximum with elevated atmospheric carbon and air pollutant levels (e.g.,
biomass production, which also depends on these characteristics. Chinese cities), factors that influence plant growth and the trim-
S. nemorosa takes a large amount of carbon in green residues to ming rate needed to maintain maximum green biomass production
the composting plant due to its natural mortality, trimming rate and by VGS.
the high dry matter percentage (Table 2 and Table S.1 in the Sup- The equations were partly drawn from the literature (e.g.,
plemental material on-line). This directly influences the amount Marchi et al., 2012; Jørgensen and Nielsen, 2015) and partly
of carbon contained in the compost produced and transferred formulated for the purposes of the model. Nevertheless, the
to agricultural soil. R. officinalis is characterized by an elevated novelty of the model is its holistic approach, in which carbon
annual carbon dioxide flow retained in the system because its stock transfer from one environmental compartment to another is
growth exceeds its natural mortality, leading to low carbon transfer considered.
from plant tissue to other compartments. By contrast, S. nemorosa The model demonstrates the advantages of vertical gardens.
contributes a large amount of carbon as green residues to the com- These structures can be installed on large surfaces (compared
posting plant, compost and agricultural soil, therefore recording to flower-beds and pots) in urban areas where little space is
the highest long-lasting carbon dioxide accumulation in the whole available.
system (all compartments). In our model, we only considered the effect of anthropogenic
Only a partial validation of the carbon stocked in soil is possible emissions due to bio-oxidation of green residues on the state vari-
because the growth and mortality rates of microorganisms (appro- ables. To evaluate a complete life cycle, it is also necessary to
priately used to avoid excessive accumulation of organic matter in consider emissions due to the fossil fuels and electricity required
soil) were in line with the values obtained by other studies (e.g., for transport of green residues to composting plants, management
Marchi et al., 2012 and Marzaioli, 2006). of the composting facility, transfer and distribution of the compost
The result of the simulation for the mixed-species set produced to the agricultural soil.
(Figs. 2 and 3), developed also for esthetic purposes, was almost It can also be used to evaluate carbon uptake by green roofs
equal to the average result of the different species (Table 1), since and other residential greenspaces in different geographical areas,
the simulation model was calibrated using the average values changing the plant species and flow diagram of the model, as well
obtained for the other models. All the state variables approached as climatic and biological parameters. Thus the model is a useful
maximum values due to the logistic growth dynamics included reference for estimating the services provided by perennial herba-
in the equations and the growth/mortality rates of plants and ceous plants in removing CO2 from the atmosphere, including in
microbial biomass, represented appropriately by time-dependent urban areas.
graphic functions. The carbon dioxide flow absorbed by the plants
and retained in the system showed a decreasing trend (Fig. 2)
because the ability of the VGS to actively absorb CO2 from the 5. Conclusion
atmosphere decreases over the years, as carbon uptake approaches
the carrying capacity of the system. On the other hand, the Carbon dioxide removal from the atmosphere by perennial
long-lasting carbon dioxide accumulating in the compartments herbaceous plants installed in a vertical greenery system was esti-
(Acc CO2 ) showed an increasing trend because the state variable is mated using a dynamic model. The model quantifies the ability
represented by a differential equation, still with a logistic dynamic, of various plants (tested separately and in a mixed-species set)
but formulated as accumulation over the years (Fig. 3). to accumulate carbon in different compartments of a sequence of
Summarizing, Table 4 and Fig. 2 suggest that the perennial processes, from the planting and growth of plants in the VGS to
herbaceous species increase in biomass over the 25 years of sim- the harvesting of residual biomass (dead plants and trimmings), its
ulation within the limits of maximum plant biomass production composting, addition to agricultural soil and assimilation by soil
(carrying capacity) of the VGS. As no long-lasting woody stock microbial biomass.
is obviously produced in VGS, trimmed and dead plant residues The model showed a CO2 uptake by plant biomass of
should be collected and composted in order to facilitate carbon 0.44–3.18 kg CO2eq m−2 of vertical garden per year. We estimated
sequestration in other compartments, such as compost, soil and that a 98 m2 VGS installed in central Italy captures an average car-
microorganisms. The dynamic model presented in this study sug- bon dioxide flow of 13.41–97.03 kg CO2eq per year. Since for esthetic
gests which of the selection of herbaceous plant species are most reasons a VGS is presumably planted with different plant species, a
efficient in creating long-lasting carbon stocks in the various com- mixed-perennial herbaceous species set (composed of S. spurium,
partments. It also identifies the carbon content in compost, soil S. nemorosa, R. officinalis, G. sanguineum, C. brunnea and F. japonica,
and microbial biomass, prompting sustainable management of equally distributed in the structure) was considered and estimated
green waste and encouraging composting of plant residues instead to capture an average carbon dioxide flow of 60.87 kg CO2eq per
of landfill disposal (IPCC, 2006). In fact, composting processes year.
determine a reduction of about 99% of anthropogenic emissions The average long-lasting carbon dioxide accumulated in the sys-
compared to organic waste disposal in landfills. tem was 219.27–1640.27 kg CO2eq per year (the highest value was
The VGS sequesters CO2 for the various compartments analyzed achieved by S. nemorosa), with an increasing trend over time, offer-
in the model (vegetation, compost, agricultural soil and micro- ing a feasible solution for climate change mitigation in cities. The
bial biomass in soil) and is therefore suitable for urban residential present model and the results obtained postulating different con-
spaces, especially if herbaceous plant services removing carbon figurations of the VGS provided evidence of carbon sequestration
dioxide from the atmosphere are maximized (e.g., Nowak and by plants as a potential environmental benefit of vegetated struc-
Crane, 2002). tures installed in urban areas. The outcomes also show that this is
We considered amounts of irrigation and nutrients suitable for possible only if the residual biomass is correctly and systematically
VGS maintenance in a Mediterranean climate and drought habitats, managed.
but these parameters can be modified to the specific environmental The model can also be used to test carbon sequestration by
and climatic conditions of other study areas. Moreover, the model is green roofs and urban residential greenspaces (e.g., flower-beds
a tool for developing management scenarios, which include inter- and lawns), adjusting the conceptual diagram, flows, parameters
actions of different nutrient and irrigation regimes. The model and equations proposed in this study, provided the green residues
can also predict carbon absorption by vegetation in megacities are composted.
M. Marchi et al. / Ecological Modelling 306 (2015) 46–56 55

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