Urban areas are rapidly expanding globally and it is expected that 60% of the world’s population will be living in cities by 2030  . Cities account for more than 70% of the energy-related to global greenhouse gases   and carbon dioxide (CO2) is one of the most abundant anthropogenic greenhouse gases contributing to increase air temperature  . The exchange of CO2 over cities is mostly governed by anthropogenic emissions originating from road traffic and local heating with natural gas, oil and coal  . As urbanization increases globally, it is becoming important to better clarify the carbon (C) dynamics of urban ecosystems  . European cities are sharing their knowledge of climate policy initiatives. In particular, London, Paris, Berlin, and Rome have signed the Covenant of Mayors including commitments to implement sustainable energy policies (e.g. increased energy efficiency and development of renewable energy sources) that meet and exceed the EU’s 20% CO2 emissions reduction objective. In addition to the energy efficiency and renewable energy sources, CO2 emissions reduction can be achieved by plants  . Plants remove CO2 from the atmosphere through photosynthesis and storing the carbon excess as biomass in roots, stems, and branches  . Nevertheless, today the relationship between vegetated urban areas and CO2 emissions reduction has not been clarified and recently only the use of plants to ameliorate urban air quality has become a focus of research   . In particular, urban areas covered by parks, gardens, tree-lined avenues, sports fields, and hedges are important sinks for CO2  . The CO2 sequestration capability is related to species, plant age and growing conditions  . Urban greening also contributes to decrease air temperature through shading, blocking wind and evapotranspiration, thus counteracting the urban heat island effects  and lowering building energy used for cooling  . Moreover, green spaces serve important social, psychological, health, aesthetic and ecological functions within urban areas  . When exposed to green areas, people show a greater well-being with physical and psychological benefits  . Among green areas, Botanical Gardens have a key role in plant conservation. The Botanic Gardens Conservation International (BGCI) defined Botanical Gardens as ‘‘Institutions holding documented collections of living plants for the purposes of scientific research, conservation, display and education’’  . There are more than 1700 Botanical Gardens worldwide  . Europe has the highest number of Botanical Gardens (527): Germany (74), France (66), United Kingdom (61), Italy (48) and the Netherlands (39)  . Botanical Gardens have a significant role in plant ex situ conservation  , taxonomic research  , horticultural and economic Botany  , public education and natural history appreciation  . Botanical Gardens also offer economic benefits associated with attracting tourists  . Some visitors appreciate the educational experiences and opportunities to view unusual or rare species, and others their role in maintaining local traditions and community identity  . In this context, we analyzed an additional role for the Botanical Gardens that should be considered, i.e. the contribution to environmental quality amelioration. In particular, the CO2 sequestration capability of the most representative plant collections developing in the Botanical Garden of Rome (Italy) and their influence on microclimate was analyzed.
2.1. The Study Area
The study was carried out in the period January-May 2016 inside the Botanical Garden of Rome (41˚53'53'' N, 12˚28'46'' E; 53 m a.s.l.). The Botanical Garden covers an area of 12 ha in the city centre, between Lungara Street and the Gianicolo Hill. The plane area is enriched with tree species, the Palm Collection and meadows, while the hill area is occupied by Ferns, Eucalyptus collection, Bamboos, Rose Garden, Japanese Garden, Rock Garden and Geophytes, Mediterranean Wood and Gymnosperms  .
The study area is under a Mediterranean type of climate. The average total annual rainfall is 848 mm, most of it distributed in autumn and winter. The average maximum air temperature of the hottest months (July and August) is 31.7˚C ± 0.1˚C and the average minimum air temperature of the coldest month (January) is 4.9˚C ± 0.9˚C. The mean yearly air temperature is 16.7˚C ± 6.5˚C (data provided by the Lazio Regional Agency for Development and Agricultural Innovation; Meteorological Station of Rome, Lanciani Street, data for the period 2006 to 2016).
2.2. Carbon Dioxide Concentration and Microclimate Measurement
Atmospheric carbon dioxide concentration (CO2, ppm), air temperature (Ta, ˚C) and air humidity (RH, %) were monitored simultaneously by handheld tools (Rotronic, CP11) along two Transects: Transect 1 from Garibaldi Square to the centre of the Botanical Garden and Transect 2 from Lungotevere della Farnesina Street to the centre of the Botanical Garden. Measurements were carried out in three different points of each transect: at the centre of the Garden (C), at 150 m from the centre (B1 and B2, for Transect 1 and 2, respectively) and outside the Botanical Garden (at 300 m from the centre, A1 at Garibaldi Square and A2 at Lungotevere della Farnesina, for Transect 1 and 2, respectively) (Figure 1). Traffic level (i.e. number of vehicles per minute) was monitored simultaneously with CO2 measurements in Garibaldi Square and Lungotevere della Farnesina Street. The sites along each transect were chosen on the base of a progressive traffic intensity decrease from street densely congested to the inner of the Botanical Garden.
2.3. Plant Collections
The most important plant collections developing in the Botanical Garden were considered. In particular, the Mediterranean Garden (2050 m2), Palms (4463 m2), Gymnosperms (15,500 m2), Bamboos (6205 m2), Mediterranean Wood (17,850 m2), Eucalyptus Collection (8500 m2), Japanese Garden (2250 m2), Erythrina Area (13,005 m2), Ferns (4250 m2), Rock Garden and Geophytes (5100 m2), Rose Garden (4250 m2) and Meadows (2423 m2) (Figure 2).
The extension of each plant collection was measured by a Quantum Gis (QGIS), an Open Source Geographic Information System (OSGEO4W, version 1.8.0) running on Windows. QGIS determines the acquisition, recording, analysis, visualization and restitution of information by geographical data. The GIS
Figure 1. The two Transects monitored from the outside to the centre of the Botanical Garden of Rome (41˚53'53'' N, 12˚28'46'' E). Transect 1: A1 (Garibaldi Square, at 300 m from the centre), B1 (at 150 m from the centre), C (centre of the Botanical Garden). Transect 2: A2 (Lungotevere della Farnesina Street, at 300 m from the centre), B2 (at 150 m from the centre), C (centre of the Botanical Garden).
Figure 2. Map of the considered plant collections inside the Botanical Garden of Rome. 1 = Mediterranean Garden; 2 = Palms; 3 = Gymnosperms, 4 = Bamboos; 5 = Mediterranean Wood, 6 = Eucalyptus Collection; 7 = Japanese Garden; 8 = Erythrina Area; 9 = Ferns; 10 = Rock Garden and Geophytes; 11 = Rose Garden.
software is useful for the census of urban green areas by the analysis of digital cartographies.
2.4. Plant Traits
Leaf Area Index (LAI) was measured by the “LAI 2000 Plant Canopy Analyzer” (LICOR Inc., Lincoln, USA) for all the considered plant collections. Structural traits of each collection, excluding Meadows, were measured on representative plants (n = 10 per plant collection). In particular, tree diameter at breast height (DBH, m) was measured by callipers (Silvanus calliper—65 cm), and a DBH tape (length = 20 m) when diameter was larger than 65 cm. Plant height (H, m) was measured by electronic clinometers (Haglöf, Sweden). The total photosynthetic leaf surface area (TPS, m2) of each plant collection was determined by multiplying each LAI value by the extension of the plant collection.
2.5. Carbon Dioxide Sequestration
The CO2 sequestration capability for each plant collection was calculated multiplying TPS by the mean yearly net photosynthesis and the total yearly photosynthetic activity time (in hours), according to  . In order to compare CO2 sequestration capability of the different plant collections, the CO2 sequestration capacity per hectare (CS, Mg CO2 ha−1∙year−1) was calculated. The total CO2 sequestration capacity of the Botanical Garden was also calculated (CSTot).
The net photosynthetic rate (NP, µmol∙m−2∙s−1) was measured by an open infrared CO2 gas analyzer (ADC LCPro+, UK), equipped with a leaf chamber (PLC, Parkinson Leaf Chamber). Measurements were made in situ on cloud-free days (PAR > 1000 µmol∙m−2∙s−1), in the morning (from 9:00 am to 12:00 pm), to ensure that near maximum daily NP was measured. On each sampling occasion, fully sun expanded leaves were used (Varone et al., 2015). Leaves were retained in their natural position during measurements. Measurements were carried out at ambient air temperature on five representative plants per each collection (three leaves per plants).
2.6. Monetary Value of CO2 Sequestration
The monetary value of CO2 sequestration for the collections growing in the Botanical Garden was estimated assuming a monetary value of $ 0.00334/lb (i.e. $0.00736/kg) for sequestered CO2, according to  .
2.7. Statistical Analysis
Differences of the means were tested by one-way analysis of variance (ANOVA), and Tukey test for multiple comparisons. Moreover, in order to understand how LAI, TPS and NP (predictors) affected CS (response variable), the predictors were combined via Principal Component Analysis (PCA) across plant collections. Then, a simple linear regression analysis between the axis explaining the largest proportion of the variance (i.e. PC1) and CS was carried out. All statistical tests were performed using a statistical software package (Statistica, Statsoft, USA).
3.1. Carbon Dioxide Concentration and Microclimate
The mean CO2 concentration during the study period was 485 ± 22 ppm (mean value of Transect 1 and Transect 2) peaking in January (522 ± 21 ppm, mean of A1 and A2) (Table 1). The highest CO2 concentration was monitored where the traffic level was the highest (31 ± 1 vehicles∙min−1, mean of A1 and A2) decreasing by 8% in May (mean of A1 and A2) associated to a 21% decrease of the traffic level (mean of A1 and A2). Along the Transect 1, A1 had a 6% lower CO2 concentration compared to A2 (Transect 2) with a 70% lower traffic level. Moreover, CO2 concentration decreased, on average, 9% from outside to the centre of the Botanical Garden in both the Transects. In particular, CO2 concentration decreased 2% and 6% from A1 to B1 and from A1 to C, respectively, along Transect 1, and 6% and 12% from A2 to B2 and from A2 to C, respectively, along Transect 2.
A similar trend was observed in Ta decreasing, on average, 14% from the outside to the centre of the Botanical Garden. In particular, Ta decreased 7% and 13% from A1 to B1 and from A1 to C, respectively, along Transect 1, and 8% and 14% from A2 to B2 and from A2 to C, respectively, along Transect 2. An opposite trend was observed for RH, increasing, on average, 7% from outside to inside the Botanical Garden (Table 1).
3.2. Plant Traits
Structural traits of plant collections are shown in Figures 3(a)-(d). The highest LAI (p ≤ 0.05) was measured in Bamboos (2.90 ± 0.06) and the lowest in Meadows (0.40 ± 0.05, mean value). The Mediterranean Wood had the highest (p ≤ 0.05) TPS (43,197 m2) and the Meadows the lowest (969 m2). DBH was the highest (p ≤ 0.05) in the Gymnosperms (1.16 ± 0.30 m) and the lowest in Rose Garden (0.06 ± 0.03 m). The Eucalyptus Collection had the highest (p ≤ 0.05) H (26.8 ± 2.3 m).
3.3. Carbon Dioxide Sequestration
Bamboos had the highest CS (210 Mg CO2 ha−1∙year−1, corresponding to 57.4 Mg C ha−1∙year−1) among plant collections, followed by the Mediterranean Wood (133 Mg CO2 ha−1∙year−1, corresponding to 36 Mg C ha−1∙year−1) while Ferns had the lowest CS (7.1 Mg CO2 ha−1∙year−1, corresponding to 1.9 Mg C ha−1∙year−1) (Figure 4). Considering the extension of each plant collection, the Mediterranean Wood had the highest CO2 sequestration capability (150 Mg CO2 year−1, corresponding to 65 Mg C year−1), followed by the Bamboos (130 Mg CO2 year−1, corresponding to 36 Mg C year−1), the Erythrina Area (110 Mg CO2 year−1, corresponding to 30 Mg CO2 year−1), Gymnosperms (109 Mg CO2 year−1,
Table 1. Carbon dioxide concentration (CO2), air temperature (Ta) and air humidity (RH) monitored during the study period (January-May) along the two Transect from the outside to the centre of the Botanical Garden of Rome. Transect 1: A1 (Garibaldi Square, at 300 m from the centre), B1 (at 150 m from the centre), C (centre of the Botanical Garden). Transect 2: A2 (Lungotevere della Farnesina Street, at 300 m from the centre), B2 (at 150 m from the centre), C (centre of the Botanical Garden). Mean values for each point during the study period are indicated in bold. The differences between the three points of each Transect were always significant at p ≤ 0.05.
corresponding to 29 Mg CO2 year−1), Eucalyptus Collection (35 Mg CO2 year−1, corresponding to 9 Mg CO2 year−1), Palms (28 Mg CO2 year−1, corresponding to 8 Mg CO2 year−1), Mediterranean Garden (17 Mg CO2 year−1, corresponding to 5 Mg CO2 year−1), Japanese Garden (15 Mg CO2 year−1, corresponding to 4 Mg CO2 year−1), Rose Garden, Rock Garden and Geophythes (10.4 ± 0.5 Mg CO2 year−1, mean value, corresponding to 2.8 ± 0.1 Mg CO2 year−1), Meadows (4.7 Mg CO2 year−1 corresponding to 1.3 Mg C year−1) and Ferns (3.0 Mg CO2 year−1, corresponding to 0.82 Mg C year−1). Considering the total extension of plant collections (8.6 ha), the CO2 sequestration capability for the Botanical Garden was of 6947 Mg CO2 year−1, corresponding to 1897 Mg C year−1.
The PCA returned two axis of variations across plant collections. In particular, PC1 was positively related to LAI and TPS accounting for 55% of the total variance. PC2 was positively related to NP accounting for 37% of the total variance. There was a significant linear regression between PC1 and CS. Nevertheless, the relationship did not hold for Gymnosperms and Bamboos collections which felt apart from the fitted line. When they were removed from the analysis, the performance of the linear model significantly increased (Figure 5).
Figure 3. Leaf area index (LAI) (A), total photosynthetic leaf surface (TPS, m2) (B), diameter at the breast height (DBH, m) (C) and plant height (H, m) (D) of plant collections growing in the Botanical Garden of Rome. Mean values ± S.E. are shown (n = 10). Mean values with the same letters are not significantly different (p ≥ 0.05).
Figure 4. Carbon dioxide (CO2) sequestration (CS, Mg CO2 ha−1∙year−1) capability of the different plant collections growing in the Botanical Garden of Rome.
Figure 5. Linear relationship between the first principal component combining LAI and TPS (PC1) and the CO2 sequestration capacity per hectare (CS, Mg CO2 ha−1∙year−1) across the Botanical Garden of Rome plant collections. The solid line represents the relationship obtained including all the plant collections (n = 12); the dashed line represents the same relationship by excluding Bamboos and Gymnosperms (n = 8; See Results section for further details). The equations, as well as their R2, are shown. The relationships were significant at p ≤ 0.05.
3.4. Monetary Value of CO2 Sequestration
The monetary value of CO2 sequestered by the Botanical Garden was 59-56$ ha−1∙year−1, to which Bamboos and Mediterranean Wood gave the highest contribution (26% and 16%, respectively), and Ferns, Rose Garden (1%) and Meadows (2%) the lowest.
Quantifying CO2 sequestration by urban vegetation is necessary for the development of low-neutral carbon cities or climate-friendly cities  . Urban green areas should include the Botanical Gardens, taking into consideration their key role of ex situ plant conservation as well as air quality amelioration capability and social benefits. The city of Rome signing the Covenant of Mayors is committed to adopt an integrated approach to tackling climate change mitigation. Thus, a better awareness of the role of urban greening in CO2 reduction achieved should be included.
On the whole, our results show that plant collections inside the Botanical Garden of Rome cover 8.6 ha corresponding to 72% of the Botanical Garden extension (12 ha). The analyzed plant collections show different structural traits. In particular, Eucalyptus and Gymnosperm collections have the highest H and DBH (26.2 ± 0.9 m and 1.16 ± 0.01 m, respectively, mean value). LAI ranges from 2.90 ± 0.06 (Bamboos) to 0.40 ± 0.05 (Meadows). LAI is an important variable for characterizing vegetation structure and function  . It is related to photosynthesis and plant biomass  . The results show that structural traits are good predictors of plant collection CO2 sequestration capability as attested by the relationship between PC1 and CS. In particular, Gymnosperms have, on average, a lower CS (70 Mg CO2 ha−1∙year−1) while Bamboos (210 Mg CO2 ha−1∙year−1) a higher, than that predicted by the linear model. Nevertheless, the two collections show the same z-score on the obtained PC1 even if strongly differed in terms of CS. The same z-score for these collections can be explained by TPS and LAI. Gymnosperms have 89% higher TPS compared to Bamboos, with the latter being characterized by a 32% higher LAI. The high net photosynthetic rates of Bamboos  explain the divergence in CS compared to the other collections and the high contribution to CSTot (26%). The lower CS of Gymnosperms compared to the other collections and the lower contribution to CSTot (9%) is linked to their low net photosynthetic rates  . Among the other collections, the Mediterranean Wood has the highest contribution to CSTot (16%), with a CS of 133 Mg CO2 ha−1∙year−1. Moreover, the Mediterranean Garden and the Erythrina Area contribute 10% to CSTot with a CS of 84 and 85 Mg CO2 ha−1∙year−1, respectively. The Rose Garden and Ferns have the lowest CS, contributing less than 2% to CSTot. Considering the extension of each collection, the Mediterranean Wood (17,850 m2) has the highest CO2 sequestration capability (150 Mg CO2 year−1) while Ferns (4250 m2) the lowest (3.0 Mg CO2 year−1). A total CO2 sequestration of 809 Mg CO2 ha−1∙year−1 is obtained for the Botanical Garden of Rome, corresponding to 221 Mg C ha−1∙year−1. There is no comparative data since there have been no other studies on Botanical Gardens. This value is in the range of the most important historical parks in Rome  . The effects of CO2 sequestration of the plant collections growing inside the Botanical Garden results in 4% CO2 reduction outside (150 m from the centre of the Botanical Garden). Moreover, plant collections decrease air temperature by 1˚C inside the Botanical Garden with positive effects on the surrounding area.
Extending the CSTot value for all the plant collections growing in the Botanical Garden of Rome, we obtain a total CO2 sequestration capability of 6947 Mg CO2 year−1, corresponding to 1897 Mg C year−1. This results in an annual economic value of 51,133$. The obtained results can suggest appropriate policy interventions in order to facilitate future urban designs enhancing the environmental and social benefits from green areas that should also include Botanical Gardens.
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