Evaluating the Ecological Services of Roof Greening Plants in Beijing Based on Functional Traits

: Selecting suitable species to enhance ecological functions is crucial for improvements in the planning and design of roof greening and in maintaining sustainable urban development, especially in rapidly urbanized areas. Assisted by ﬁeld trips to enhance studies, the present project assessed the ecological functions of 207 plant species used for roof greening in Beijing based on their key functional traits. The results indicate that regulating, cultural, supplying, and supporting functions di ﬀ ered signiﬁcantly among species and families in the study area. Rosaceae species have higher levels of overall ecological functions than other species, and a large number of Compositae species have lower-level functions. Compared to other families, Araliaceae and Nyctaginaceae have higher mean values of cultural and supporting functions and the highest mean overall function value of 37. , Berberidaceae , and Aceraceae have higher mean regulating, cultural, supporting, and overall function values. Amaranthaceae , Umbelliferae , Lamiaceae , Saxifragaceae , Ericaceae , and Gramineae have lower values. The existing roof greening in Beijing includes some pitfalls with respect to plant composition as well as plant selection that does not consider ecological functions. The following measures could be proposed to increase ecological functions: (1) Increasing the number of plants with shallow roots and with strong adaptation traits to roof conditions; (2) Enriching ecological communities with diverse plants with high ecological functions; and (3) Carrying out rational ecological planning and management based on detailed and objective data on plant species. Future studies should focus on specifying plant functional traits to enhance ecological functions.


Introduction
Roof greening refers to planting on top of buildings or on elevated platform areas including roofs, terraces, and podiums, as well as on aerial platforms and overpasses that are not directly connected to natural soil on the ground [1]. It is usually divided into three categories: extensive, semi-extensive, and intensive [2,3]. Extensive green roofs have a characteristic shallow substrate of <15 cm in depth, and are usually covered with herbaceous or low-shrub plants that are tolerant to environmental stresses, tolerant to mowing or pruning, demand little or no irrigation, and require little maintenance. Intensive green roofs integrate green function and leisure function as a whole. Their substrate is deep and they can support woody plants including trees and shrubs accompanied by herbaceous ground-level vegetation, most of which is ornamental [4]. Semi-extensive green roofs have characteristics lying between the above two categories, and may offer a combination of environmental and aesthetic benefits [5].
formulation, and development, construction, and maintenance methods [50]. Thus, Beijing has great potential for developing roof greening to improve its ecological environment. On a more practical level, whether the current roof greening plants provide adequate support for ecological services has not been adequately investigated. Furthermore, few studies touch on the assessment of all the four sets of ecological functions in the context of the relatively comprehensive ecosystem services that could be provided by roof-greening plants.
Based on field investigations, classification systems of plant functional traits [24][25][26][27], the Millennium Ecosystem Assessment (MA) ecosystem service function classification [8], and other related studies [40], this study probes plant functional traits and evaluates the ecological functions of roof greening plants in Beijing. From the findings, useful recommendations found for plant selection and ecological-function enhancement are provided to improve the planning and design of roof greening and maintain sustainable urban development, especially in rapidly urbanized areas.

Study Area
Beijing is located at 39 • 23 N-40 • N, 115 • 20 E-117 • 30 E with an area of 16,410.54 km 2 and a population of 21.73 million [51]. It has a continental monsoon climate with a cold and dry winter and a mild and moist summer. The annual mean precipitation is 682.9 mm and the frost-free period lasts 150-180 days [52]. The species diversity in urban greening is high. The plants are dominated by species of the tropical region, the northeastern cold zone, and Siberian flora [53]. At the end of 2017, the per capita public green space in Beijing was 16.2 m 2 [51]. The total roof area was about 200 million m 2 , and the roof greening area reached more than 2 million m 2 [54]. Roof greening has been verified to improve the microclimate of roofs in Beijing by decreasing the mean temperature by 2-3 • , decreasing the wind velocity from 0.32-2.70 m/s to 0.40-1.11 m/s and increasing the relative humidity by 2.7% [55].
We collected our species information by following four steps. First, we used digital maps to locate the positions of roof greening. Second, we carried out field studies to collect data on species planted on roofs. Third, we searched the literature to assemble more data on plant species grown on green roofs in Beijing. Fourth, we built a database to analyze the data.
The Getscreen auto-screen mosaic tool was first used to capture a Google Earth satellite image and retrieve the Geotiff format image in 2014. Then the grid image in Geotiff format was loaded into ArcGIS for digitization, and the spatial distribution map of roof greening within the Beijing Fifth Ring Road was obtained. From 201 objects, 51 plots were successfully reached and surveyed in field trips in August 2014. We investigated the characteristics of plant composition and the functional traits of each plant. We investigated the following aspects: (1) Characteristics of the surroundings, such as land use type, geographical location, and location layer in the building; (2) Characteristics of the roof greening, including types of roof greening, soil depth, and green ratios on the roofs; and (3) Plant information, including species name, number, height, etc.

Classification of Plant Functional Traits and Ecological Functions
Based on field investigations and assisted by the Global Plant Functional Attribute Classification System Handbook [26], Flora of Beijing [57,58], we summarized a list of plant functional traits (Table 1) by sorting the floristic composition of 207 plant species used for roof greening in Beijing. The key  The parameters of the selected traits  and their relationships with different ecological functions were set up (Table 2). A weight was assigned to each functional trait based on the number of its ecological functions (regulating, cultural, supporting, and supplying) ( Table 3). The ecological function value of each plant was calculated by the following formula: where EF is the ecological function value of each plant; i is the functional trait; P are the parameters of each plant's functional traits; and W is the weight assigned to each functional trait.
Growth adaptability [40] 1. Single adaptability (1); 2. Multiple adaptability (2-3); 3. Comprehensive adaptability (4 and more) Plants with more growth adaptations tend to have higher environmental regulating abilities such as decreasing temperature and air pollution, and increasing humility. They can be widely used in most roof greening and provide more supporting functions such as for wildlife habitats.

Distribution of Roof Greening in Beijing
All 201 roof greening sites and the surveyed 51 plots are displayed in Figure 1. The site number and per cent of roof greening in each district are listed in Table 4. It can be inferred from Figure 1 and Table 4 that most existing roof greening and surveyed plots are concentrated in four districts: Haidian, Chaoyang, Dongcheng, and Xicheng, which are more densely populated and have more intense urbanization than other districts. Xicheng and Chaoyang contribute over half of the total number and area of roof greening sites.

Distribution of Roof Greening in Beijing
All 201 roof greening sites and the surveyed 51 plots are displayed in Figure 1. The site number and per cent of roof greening in each district are listed in Table 4. It can be inferred from Figure 1 and Table 4 that most existing roof greening and surveyed plots are concentrated in four districts: Haidian, Chaoyang, Dongcheng, and Xicheng, which are more densely populated and have more intense urbanization than other districts. Xicheng and Chaoyang contribute over half of the total number and area of roof greening sites.   The surveyed plots of roof greening were classified into extensive roof greening, extensive platform greening, intensive roof greening, and intensive platform greening. The number of greening types in the field investigation and their ratios are shown in Table 5. It can be inferred from Table 5 that greening on roofs and extensive greening occupied more than 75% of the total plots. The plots were usually located in hospitals, schools, commercial districts, residential areas, government offices, etc. Among these, the commercial area has a higher availability of roof greening with plants that are more recreational and ornamental in nature. Most government office areas have extensive roof greening with low accessibility. In hospitals, both extensive and intensive roof greening exist. Intensive roof greening provides patients and their families with leisure and entertainment services, whereas extensive roof greening is almost impossible to reach in most cases. In residential areas, most public greening is on a platform within the community. The public platform greening always plants on a high platform for amusement or for parking, as seen in the intensive platform greening of Wangjing Garden and Jianwai SOHO (small office, home office). Private roof greening in residential areas has not been included in this field investigation. From long-distance visual observation its plant composition is rich and beautiful with high entertainment value, but it only serves the residential area owners.

Taxonomic Characteristics of Roof Greening Plants
According to the field investigation and related literature [48], 207 plants used in Beijing roof greening are summarized (see Supplementary Materials). They belong to 161 genera from 61 families (Supplementary Materials). It can be inferred from the Supplementary Materials that Compositae has 31 species from 24 genera, occupying 15%; Rosaceae has 21 species from 12 genera, occupying 10%; Gramineae has 13 species from 13 genera, occupying 6%; and Cupressaceae has nine species from five genera, occupying 4%. Crassulaceae sp., Cucurbitaceae sp., Leguminosae sp., Oleaceae sp., Chenopodiaceae sp., Lamiaceae Martinov sp. and Convolvulaceae sp. occupy 3% of the plants. Each of the other families account for less than 3% of the plants.

Functional Traits of Roof Greening Plants
According to the characteristics of plant functional traits listed in Table 2, a large number of roof greening plants in Beijing are phanerophytes (76 species, 58% of the total, dominated by Cupressaceae sp. and Rosaceae sp.) and therophytes (61 species, 29% of the total, dominated by Compositae sp., Cucurbitaceae sp. and Gramineae sp.). Most are herbaceous plants (119 species, 58% of the total, dominated by Compositae sp. and Gramineae sp.), perennial species (144 species, 70% of the total, dominated by Rosaceae sp., Compositae sp., and Cupressaceae sp.), and those with a faster growing rate (201 species, 97% of the total). They often have cauline leaves and multiple stems and branches, such as Ixeridium sonchifolium (Maxim.) Shih of Compositae and Buddleja davidii Franch. of Loganiaceae. Most plants have strong adaptation and are tolerant to the cold, heat, drought, and wind. They usually also have multiple supplying values, especially medicinal, gardening, and economic value, such with Sedum lineare Thunb. of Crassulaceae, Ixeridium chinense (Thunb.) Nakai of Compositae, and Agrimonia pilosa Ldb. of Rosaceae.
Most plants are deciduous (178 species, 86% of the total), and the senescence period is mainly in autumn (122 species, 59 of the total). Most leaves of the plants are small (94 species, 45% of the total). The texture of the leaf is mostly papery (111 species, 54% of the total) and not fleshy (197 species, 95% of the total). The leaf color is mostly green (194 species, 94% of the total).
The flower color of 30% of plants is yellow (62 species). The anthesis of most plants is in the summer (64 species, 31% of the total) or the summer-autumn transition season (62 species, 30% of the total). There are 12 species where the anthesis lasts 5 months or longer. The fruit period is always in autumn (99 species, 48% of the total) and approximately seven species have a fruit period of more than 5 months.
Most plants have shallow roots (188 species, 91% of the total, dominated by Compositae sp., Rosaceae sp., and Gramineae sp.), and have no underground organ to store nutrients (160 species, 77% of the total, dominated by Rosaceae sp., Compositae sp., and Gramineae sp.). A few plants have fleshy roots (Sedum sarmentosum Bunge of Crassulaceae), root tubers (Cirsium japonicum Fisch. ex DC. of Compositae), and rhizomes or tubers.
The propagating methods of the plants are diverse. Most plants have more than one propagation method. They usually select entomophily (141 species, 68% of the total, such as Compositae sp., Rosaceae sp., and Crassulaceae sp.) as the main method, because most of such plants have nectar and pollen (131 species, 63% of the total).

Ecological Functions by Roof Greening Plants
The relative values of ecological functions calculated by the different functional traits of the plants are listed in Supplementary Material Table S1. Based on this, a comparison chart of four ecological functions is obtained (Figure 2).

Ecological Functions by Roof Greening Plants
The relative values of ecological functions calculated by the different functional traits of the plants are listed in supplementary material Table S1. Based on this, a comparison chart of four ecological functions is obtained (Figure 2).  Table 6 shows the mean values of plant ecological functions in different families. It can be inferred from Table 6 that about eight families have the highest mean regulating function values as compared to other families, at ≥11. These are Buxaceae (11), Ulmaceae (12), Rhamnaceae (11), Aceraceae (11), Moraceae (11), Buxaceae (11), Celastraceae (11), Sapindaceae (11), and Ginkgoaceae (11). Solanaceae, Apiaceae, Oxalidaceae, Calycanthaceae, Labiatae, Liliaceae, and Amaranthaceae have the lowest mean regulating function value of 7. Araliaceae and Nyctaginaceae have the highest mean cultural function values of 13 and 11, respectively. In addition, Gramineae and Amaranthaceae have the lowest mean cultural function value of 5. Eight families have the highest mean supporting function values at ≥11. They are Nyctaginaceae (15), Loganiaceae (13), Araliaceae (12), Lythraceae (11), Bignoniaceae (11), Ulmaceae (11), Berberidaceae (11), and Verbenaceae (11). Gramineae (6), Apiaceae (6), and Amaranthaceae (5) have the lowest mean supporting function values at ≤6. Overall, 51 families have a mean supplying function value of 2, and 10 families have a mean supplying function of 1. There are 39 families that have a higher total function value than the mean value of 26.9, of which Ulmaceae has the highest value of 37, followed by Sapindaceae and e with a value of 35, and Berberidaceae and Aceraceae with a value of 34. Labiatae has the lowest total function value of 20, followed by Amaranthaceae and Saxifragaceae with a value of 21.  The key aim of this paper was to reveal the ecological function values of Beijing roof greening plants by analyzing their functional traits. Inferred from the analyses, the following problems exist in Beijing's roof greening plants. Firstly, the composition structure of roof greening plants is unreasonable. Although 161 species of plants from 61 families are applied to roof greening, the number of plants from different families varies greatly. For example, the number of Compositae sp. accounts for 44% of the total, and about 50 families make up less than 3% of the total as a whole. This is also a common problem in the current roof greening in China. For example, the survey on roof greening in Pu'er City, Yunnan Province, showed that the local form of roof greening is singular and the ecological benefits are not maximized [66]. A survey on roof greening in Lanzhou, Gansu Province, showed that the local roof greening plants are not properly selected. The types are simple and seasonality is lacking [67]. Another survey found that Chongqing has abundant plant resources, but insufficient plant species are used in roof greening [68]. Secondly, the selection of plants does not consider the ecological functions. For example, many species of Compositae and Gramineae are used in roof greening, but their ecological function levels are low. The overall ecological function levels of Berberidaceae and Sapindaceae are high, but their species are deficient.

Plant Ecological Functions in Different Families
The future construction of roof greening in Beijing should focus on plants with high values in ecological function. The following are suggestions for improvement. Firstly, a possible course of action is increasing the numbers of plants that are strong at adaptation and have shallow roots, especially those tolerating wind, cold, drought, heat, and barren habitats, such as Sedum lineare Thunb., Sedum sarmentosum Bunge., Malus spectabilis (Ait.) Borkh., Amygdalus persica L. var. persica f. duplex Rehd., and Hedera nepalensis var. sinensis (Tobl.) Rehd. Most Crassulaceae sp. have good drought resistance through drought stress and other means [69]. Plants with deep roots such as Wisteria sinensis, Ulmus pumila L., and Morus alba L., are not suitable for planting on roofs. A second suggestion is enriching the ecological community and diversifying the species of herbaceous plants, shrubs, and lianas with high ecological functions. Sedum lineare Thunb. is the most widely used vegetation roofing material. However, due to long-term single planting and lack of cultivation, problems such as baldness, degeneration, and death are prominent. Among the species that belong to Crassulaceae sp., the drought-resistant perennial flowers are a large class of roof plants and should be studied deeply for future planting in roof greening [44]. More plants with rich colors and long florescence can be cultivated, such as Chaenomeles speciosa (Sweet) Nakai, Cerasus yedoensis (Matsum.) Yu et Li, and Rosa chinensis Jacq. Native plants with colorful leaves or evergreen native plants can be considered as well. For example, Berberis thunbergii var. atropurpurea Chenault has purple-red leaves, and Cedrun deodara and Ilex ficoidea Hemsl. var. parvifilia S. H. Fu var are evergreen. A third suggestion is carrying out rational ecological planning and management of roof greening to enhance ecological function levels [7]. Ecological planning includes the connection between the composition structure and distribution characteristics of plants and the regional ecosystem. Ecological management includes advanced ecological engineering technology, an appropriate management system, and the training of professional managers.
Screening suitable species is necessary for successful greening on roofs, where there are often extreme environmental conditions such as high illumination intensity, long illumination time, high-temperature differences between day and night, low air humidity, high wind speed, and a thin soil layer. This study indicated that the functional traits of roof plants are closely related to the roof environment. Usually, roof plants characterized by small leaves, short and shallow roots, fast growth rate, and diverse breeding methods are tolerant to cold, heat, drought, and wind. Thus, characterizing plant functional traits is an efficient way to predict their functions or services for various purposes in roof greening, without considering geographic distribution, ecological niche, and taxonomic/phylogenetic relationships [7]. Each type of ecological function has many detailed perspectives. One single plant functional trait may not be enough to reflect each ecological function. Thus, in order to get relatively accurate values of ecological functions, a set of related plant traits should be considered.
This study is helpful in green roof establishment for several reasons. Firstly, it has theoretical meaning because it assesses all the four ecological functions such as regulating, supporting, cultural, and supplying functions using a relatively comprehensive set of functional traits of plants on roof greening, and evaluates the differences of each function by plants and families. Secondly, it has practical meaning because it provides conclusions on the problems occurring in Beijing roof greening and provides useful information about screening suitable species and enhancing ecological functions. Because of the large amount of data and high technical requirements, more studies should be performed in the future to specify plant functional traits and to evaluate more detailed ecological functions such as regulating temperature and humidity, alleviating air pollution, conserving water, enhancing aesthetic, entertainment, and spiritual functions, and providing nutrient circulation, as well as medicinal, gardening, and economic value.  (1)).

Conflicts of Interest:
The authors declare no conflict of interest.