Urban green spaces as potential habitats for introducing a native endangered plant, Calycanthus chinensis

Urban Forestry & Urban Greening 46 (2019) 126444

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Original article

Urban green spaces as potential habitats for introducing a native endangered plant, Calycanthus chinensis

T

Kaixuan Pana,1, Yijun Lua,b,1, Shuonan Hea, Guofu Yanga, Yi Chena, Xing Fana, Yuan Rena, Meng Wangc, Kangdi Zhua, Qi Shend, Yueping Jiange, Yan Shif, Panpan Mengg, Yuli Tangh, ⁎ Jie Changa, Ying Gea, a

College of Life Sciences, Zhejiang University, 866 Yuhangtang Road, Hangzhou, 310058, PR China Hangzhou Botanical Garden, 1 Taoyuanling, Hangzhou, 310013, PR China c State Environmental Protection Key Laboratory of Wetland Ecology and Vegetation Restoration, Institute for Peat and Mire Research, Northeast Normal University, Changchun, 130024, PR China d Zhejiang International Studies University, 140 Wensan Road, Hangzhou, 310012, PR China e Xixi National Wetland Park Reasearch Center for Ecological Sciences, Xixi National Wetland Park, 518 Tianmushan Road, Hangzhou, 310013, PR China f School of Landscape Architecture, Zhejiang A & F University, Lin’an, 311300, PR China g College of Biological and Brewing Engineering, Taishan University, Yingbin Road, Taian, 271021, PR China h Hangzhou West Lake Scenic Area Management Committee, 1 Longjing Road, Hangzhou, 310013, PR China b

A R T I C LE I N FO

A B S T R A C T

Handling Editor: J. Jun Yang

Ex situ conservation in urban areas is an essential complementary approach to in situ conservation in wild areas. In this study, we combined multiple approaches, including vegetation investigations for both natural habitats and urban green spaces, eco-physiological experiments and remote sensing investigations for urban green spaces, to identify potential habitats for introducing the endangered plant species Calycanthus chinensis to urban green spaces. The results showed that (1) C. chinensis prefer living under sparse forests with canopy densities of 20–60%; (2) C. chinensis was not a shade tolerant species due to its chlorophyll a/b ratio (2.58) being higher than the threshold (2.3) for shade tolerant species; (3) the large and thin leaves of C. chinensis are easily damaged by strong wind, so this species can only live under moderate canopy cover; (4) to maintain a sparse crown for the well-being of C. chinensis, the upper layer trees in urban green spaces need to be thinned slightly; and (5) introducing this endangered species increases biodiversity and ecosystem services of urban green spaces. Finally, this study provides a framework and a case study for using urban green spaces as micro-refuges for endangered species.

Keywords: Conservation Eco-physiological traits Functional traits Habitat preference Micro-refuges Realized niche

1. Introduction The loss of natural habitats is a primary driver of species decline (Noss et al., 2012; Gibb and Cunningham, 2013; Maxwell et al., 2016; Johnson et al., 2017). The natural habitats of many species, especially endangered species, are threatened due to extensive human disturbances and global changes in their distributions (Laurance, 2012; Li and Pritchard, 2009; Virkkala et al., 2013; Johnson et al., 2017). The ex situ conservation has been considered an essential approach for conserving endangered plant species besides in situ conservation (Li and Pritchard, 2009). The identification of various suitable habitats for ex situ conservation to protect endangered species is urgent (Harrisson et al., 2012; Watson et al., 2011).

Conserving endangered species in urban areas has been recognized as a complementary approach to in situ conservation (Alvey, 2006; Varese et al., 2011). Urban green spaces have expanded rapidly worldwide in recent decades (Fuller and Gaston, 2009). In particular, these spaces are historical distribution areas of many endangered species and share the same climatic conditions as native habitats (Fan et al., 2016). Notably, the diverse habitats in green spaces can meet various demands of different species (Godefroid et al., 2007; Madre et al., 2014). Therefore, urban green spaces have the potential to provide habitats for protecting endangered species. The introduction of endangered plants to urban green spaces is meaningful to endangered species conservation. In addition, this approach would also contribute to increasing species richness and phylogenetic differences as well as

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Corresponding author. E-mail address: [email protected] (Y. Ge). 1 These authors contributed equally to this study. https://doi.org/10.1016/j.ufug.2019.126444 Received 18 April 2019; Received in revised form 28 August 2019; Accepted 29 August 2019 Available online 29 August 2019 1618-8667/ © 2019 Published by Elsevier GmbH.

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decreased rapidly because many habitats have changed in recent decades. The species has been recorded as an endangered species in "China Species Red List" since 1991 (Fu and Chin, 1992). Alternative ways to conserve this species in addition to in situ conservation must be found. This species has high ornamental value due to its beautifully shaped flowers with white or purple-red colours. The flowering season (May) is different from that of most other trees and shrubs in the family Calycanthaceae (flowering season in October – February next year) in this area. Therefore, it has a high aesthetic value in urban areas. Hangzhou city is located within the natural distribution area of C. chinensis. In 2014, the built-up area of Hangzhou city was 495 km2. The area of urban green spaces was ∼200 km2, of which the green spaces in parks were 63 km2, accounting for 31% of the urban green spaces (Hangzhou Statistical Yearbook, 2014). In this study, Hangzhou city was used as the study area for introducing C. chinensis to urban green spaces.

promoting ecosystem services in urban areas. Furthermore, such introductions will also increase species evenness and γ-diversity (Meffin et al., 2010) at the regional scale. To date, only a few endangered tree species (for example, Ginkgo biloba L., Metasequoia glyptostroboides Hu & W. C. Cheng, and Liriodendron chinense (Hemsl.) Sarg.) have been successfully introduced to urban areas for ornamental use. These species are introduced to cities not only within their native distribution ranges, but also outside their native ranges (Zhu et al., 2019). However, case studies on introducing endangered shrub and herb species to urban green spaces are lacking. For endangered species, each species has a specific habitat preference, and its niche is usually narrower than that of common species (Manel et al., 1999; Guisan and Thuiller, 2005). There have been many studies on the eco-physiological mechanisms of endangered plants (Liu et al., 2006; Fahad and Bano, 2012; Fan et al., 2016). For urban areas conserving endangered species, some studies have focused on investigating existing endangered plants (Ives et al., 2016) or how various habitats affect endangered species (Kümmerling and Müller, 2012). However, few studies combine the habitat requirements of endangered plant species with the features of urban green spaces. The study of the principle and methodology of introducing endangered plant species to urban areas is still rare. To determine the potential habitats in urban green spaces for endangered species, multidisciplinary studies are needed. In this paper, we carried out a multidisciplinary study to identify the potential habitats for introducing an endangered shrub, Calycanthus chinensis Cheng et S. Y. Chang, to urban green spaces. This multidisciplinary study included vegetation investigations of wild forests and urban green spaces, a common garden experiment and a remote-sensing investigation for urban green spaces. The aims of this study are to (1) develop a framework to identify potential habitats for introducing endangered plant species to urban green spaces; (2) measure physiological and functional traits that indicate the preferences for environmental factors of C. chinensis; (3) assess the probability of the potential habitats for conserving C. chinensis in urban green spaces; and (4) analyse the benefits of introducing endangered plant species to urban green spaces.

2.3. Field investigation and common garden experiments In this study, both field and common garden experiments were conducted to explore the habitat preference of C. chinensis. In the field, C. chinensis was found in low mountainous, hilly areas or basins, and it was mainly found in forests. In the field investigation, we set up five plots (10 m × 10 m) randomly at each research site (five sites in total, Table 1, Fig. 3a). We then measured the canopy density of the tree layer, distance from the forest edge of C. chinensis individuals, and height, leaf number per branch and number of branches of each individual of C. chinensis. The growth status (i.e.survival/death and whether leaves are broken) of the individuals in the five sites were also recorded. Based on the field observations, C. chinensis was mainly dispersed under sparse forests. Common garden experiments were carried out to measure the eco-physiological and functional traits of C. chinensis. This method is an effective way to study endangered species by comparing certain characteristics with those of congeneric non-endangered species (Chang et al., 2004; Fan et al., 2016). Thus, we chose the most closely related species Chimonanthus praecox (Linn.) Link and Ch. salicifolius Hu, which are within the same family as C. chinensis for comparison. The distribution areas of these three species overlap in their natural distribution, but C. chinensis has the smallest geographic range (Fig. 2). All of the individuals of the three species used for the eco-physiological experiments were grown in the plant classification section of Hangzhou Botanic Garden (30° 15′ N, 120° 16′ E). According to the accession records from Hangzhou Botanic Garden, the individuals of C. chinensis were introduced to the garden in 1964. The individuals of Ch. praecox and Ch. salicifolius were introduced to the garden in 1957 and 1958, respectively. Furthermore, by reproduction, over 800 individuals of C. chinensis were colonized (Fig. 3c), and some of them have been transplanted to other botanical gardens in China and other countries. The habitats these species grew in were similar to the wild habitats through artificial configuration, considering canopy density and community structure. The survival rates of the individuals at three sites were also recorded in this study. In June 2014, the eco-physiological traits (light saturation point, light compensation point, and maximum net photosynthesis rate) of five marked individuals of each species were measured in the plant classification section. To obtain the light response curves, the net photosynthetic rates were measured using a Li-6400 portable steady porometer (Li-Cor, Lincoln, USA) with a photosynthetic photon flux density gradient of 0, 10, 20, 50, 100, 200, 500, 1000, 1500 and 1700 μmol m−2 s−1. The chlorophyll content was extracted using ethanol and ethane (Peng and Liu, 1992) and then determined by a spectrophotometer (HP 751, Hewlett Packard, Shanghai, China) at wavelengths of 663 and 645 nm. Ten individuals of each species were marked and measured to obtain functional traits, including leaf number per branch and number of

2. Materials and methods 2.1. A framework for studying and introducing practices This research is based on multidisciplinary works, and we developed a research framework (Fig. 1). The framework includes six steps: (1) field investigation for vegetation in wild areas where the endangered plant species are distributed and determine the preferences for environmental factors based on preliminary field work; (2) common garden experiment to test the preference for certain environmental factors of the endangered plant species based on the assumptions in step 1; (3) analysis to extract the habitat preference of the endangered plant species by combining the results from the field work and common garden experiment; (4) investigation of urban green spaces, including remote sensing and ground investigation, for habitat characteristics and spatial distribution; (5) assessment of potential habitats of the endangered plant species in urban green spaces by synthesizing steps 3 and 4; and (6) evaluation of the invasive risks for introducing this species to urban green spaces. 2.2. Characteristics of C. chinensis and its habitats The endangered species C. chinensis is a shrub species that belongs to the family Calycanthaceae. It is distributed in the humid subtropical region of China and is limited to a narrow area in eastern China (Fig. 2). The region has a warm and moist subtropical monsoon climate, which occurs from spring to autumn. The mean annual temperature is 13–15 °C, and the mean annual precipitation is approximately 1500 mm. In natural habitats, the population of C. chinensis has 2

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Fig. 1. Research framework for introducing an endangered plant species to urban green spaces. It is a multidisciplinary framework involving field investigation, common garden experiments, remote sensing and community investigation for urban green spaces.

2008), we obtained a 20 m × 20 m grid overlaid with the layer of blockshaped green spaces in parks, where each grid was a quadrat. We identified 1452 quadrats and classified them into 4 levels based on the canopy density by visual interpretation of remote sensing images (Chang et al., 2017). The four levels were dense forest with canopy densities of 80%–100%, middle dense forest with canopy densities of 60%–80%, sparse forest with canopy densities of 20%–60% and open field with canopy densities of 0%–20%. The frequency of each canopy density (FHi) was calculated as:

branches. Leaf samples were taken, and the leaf area was determined by Win FLORA Pro 2002a (Regent Instruments INC, Quebec, Canada). The samples were oven-dried at 65 °C for 48 h to constant weight, and then, the biomass was measured. 2.4. Urban green spaces investigation and data collection In cities, block-shaped green spaces, which have a width greater than 20 m in parks, were chosen for determining the habitats suitable for C. chinensis in this study. This type of green space is relatively less fragmented, undisturbed by humans, and rarely converted to other land-use types (Chang et al., 2012). In this study, the urban green space investigation was conducted in Hangzhou city. The block-shaped green spaces in the parks were investigated by both remote sensing and ground measurements. For the remote sensing approach, we created a map layer of block-shaped green spaces in parks using high-resolution aerial images of Google Earth™ (https://www.google.com/earth/) through visual interpretation. We used images during the summer season because the canopy density can be accurately identified, and the target species C. chinensis flourishes in summer. Using ArcMap 9.3 (Esri,

FHi =

Ni Nt

(1)

where Ni is the number of quadrats with canopy density level i; Nt is the total number of investigated quadrats. To verify the accuracy of the canopy density measured in Google Earth, more than 10% quadrats (n = 159, Fig. 3b) were randomly selected for ground measurement and verification (Fig. 3d). In each quadrat, the habitat characteristics were investigated. The tree species were recorded, and the canopy density of the trees was measured by a photography method (Chang et al., 2017) and then, the coverage of the 3

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Fig. 2. Natural distribution areas of Calycanthus chinensis (red ellipse) and two related species, Chimonanthus praecox (green ellipse) and Chimonanthus salicifolius (blue ellipse). All three species are endemic to China.

2.5.3. Tree diversity in urban green spaces The Shannon-Wiener index (H) and Simpson index (DS) in green spaces were calculated as follows:

tree canopy was calculated. 2.5. Calculation and data analysis

n

H = − ∑ Pi lnPi

2.5.1. Eco-physiological and functional trait calculations The light saturation point, light compensation point, and maximum net photosynthesis rate were determined according to the methods of Bassman and Zwier (1991) and Zhou et al. (2010). The functional traits, including area per leaf (cm2) and specific leaf area (SLA, cm2 g−1), were determined by following the methods of Hunt (1982).

n

DS =

(4)

where Pi is the importance value of species i in each quadrat. Statistical analysis was performed in SPSS 13.0 for Windows (SPSS Inc., Chicago, IL, USA). The least significant difference test for comparing eco-physiological and functional traits was performed on each variable when there was a significant treatment effect after the ANOVA. Statistical significance was determined at α = 0.05.

n

∑ FHi ×SRi

∑ Pi2 i=1

2.5.2. Potential habitats for C. chinensis introduction to urban green spaces The probability of potential habitats for C. chinensis (PHc) in blockshaped green spaces in the parks was calculated as:

PHC =

(3)

i=1

(2)

i=1

where FHi is the frequency of habitats with canopy density level i; SRi is the survival rate of C. chinensis in this type of habitat. Table 1 Sample points in field investigation for Calycanthus chinensis. Location

Qingliangfeng Qingliangfeng Qingliangfeng Qingliangfeng Tiantai

30 30 30 30 28

º02 º02 º11 º03 º59

′N, ′N, ′N, ′N, ′N,

118 118 119 118 120

º59 º55 º01 º41 º49

′E ′E ′E ′E ′E

Crown density of tree layer (%)

Height of Calycanthus chinensis (m)

Distance from forest edge (m)

55 62 75 58 53

1.56 1.54 1.32 1.37 1.58

17.5 ± 2.3 12.7 ± 1.0 10.9 ± 1.2 6.5 ± 1.3 12.6 ± 1.7

± ± ± ± ±

7 5 1 1 17

4

± ± ± ± ±

0.49 0.34 0.35 0.37 0.32

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Fig. 3. Locations of the five sampling sites for field investigation (a), the 159 sampling quadrats for validating the accuracy of canopy density measured by remote sensing (b), three sites with introduced Calycanthus chinensis in Hangzhou Botanical Gardens (c), and the relationship between the canopy density in green spaces determined by remote sensing and field investigation (d).

species is not a shade-tolerant species. However, our field investigation showed that this species was not found at forest edges or in open fields but grew under sparse forests. The theoretical niche measured by the eco-physiological experiment was different than the realized niche of this species, so further analysis is needed. The functional traits of C. chinensis explained the difference between the theoretical and realized niche to some extent. The specific leaf area and area per leaf of C. chinensis were large, but the number of leaves per individual and leaf area per branch were small (Fig. 5a, Table 2). Large and thin leaves have high light capture ability but are easily destroyed by wind (Gardiner et al., 2016). In open field habitats, many leaves of C. chinensis were damaged after strong winds in both the field and Hangzhou Botanical Garden (Fig. 5b–d). This result can explain the discrepancy between the preference for high light and the realized niche (under sparse forest) of C. chinensis. The discrepancy may have occurred because of the species in this study, C. chinensis has the smallest leaf number, and damage to some leaves of C. chinensis would significantly decrease the total photosynthesis (Richards, 2000). This result verified that the niche of endangered plant species is usually narrower than that of common species (Manel et al., 1999; Guisan and Thuiller, 2005). The narrow niche of C. chinensis indicated that there is a trade-off (Tilman, 1982; Litchman et al., 2007) between light preference and wind damage resistance of C. chinensis. The ideal shelter for this species is under sparse forests with canopy densities of 20%–60%. Furthermore, the high mortality of C. chinensis individuals in the open fields also supports the conclusion.

3. Results and discussion 3.1. Theoretical niche and realized niche of C. chinensis In its natural habitats, C. chinensis often grows under evergreen and deciduous broadleaved forest, with a community height varying from 10 m to 14 m. As a shrub, C. chinensis is approximately 1.32 m–1.58 m in height (Table 1). Vertically, this species was located in the middle or near the ground surface of the forest. Horizontally, C. chinensis was distributed within the forest and far from the forest edge, at 12 m on average and with an upper tree canopy density of 53%–75% (Table 1). Since the 1950s, C. chinensis has been introduced to botanical gardens in several cities, and the first case was in Hangzhou Botanical Garden. In Hangzhou Botanical Garden, the C. chinensis under a tree canopy density of 20%–60% had a much higher survival rate than under other canopy densities (Fig. 4a). The eco-physiological experiment showed that the light compensate point, light saturation point, and the maximum net photosynthetic rate of C. chinensis were higher than that of Ch. praecox but lower than that of Ch. Salicifolius (Fig. 4b). This result means that there are no significant differences between endangered plant species and the other two common species in terms of these traits. Therefore, the response of photosynthesis to light intensity cannot account for endangered species mechanisms or its special habitat requirements. In contrast, the chlorophyll a/b ratio of C. chinensis was 2.58, which was significantly higher than those of the other two species, 1.75 and 1.20, respectively (Table 2). The chlorophyll a/b ratio of leaves indicates the light-harvesting capacity and the light preference of a species (Dale and Causton, 1992). Chlorophyll a/b at 2.3 is considered the critical threshold for distinguishing light preference and shade tolerant species (Johnson et al., 1993). The chlorophyll a/b ratio of C. chinensis indicated that this

3.2. Introducing C. chinensis to urban green spaces Table 3 shows the frequency of different canopy densities of blockshaped green spaces in urban parks. Furthermore, based on the findings 5

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Fig. 4. Survival rate of Calycanthus chinensis under different canopy densities (a), the net photosynthetic rate (means ± SE) of Calycanthus chinensis and two related species (Chimonanthus praecox and Chimonanthus salicifolius) in response to photosynthetically active radiation (b).

urban parks, including forest, lawns, wetlands, and riverbanks, can provide micro-refuges for different rare and endangered species. For example, a study found that the endangered species Rosa jundzillii prefers living in habitats away from the edges of park forests, while ecotones and dry grasslands are good habitats for Geranium phaeum L. in gardens (Kümmerling and Müller, 2012). This finding indicated that green spaces with large areas and diverse habitats in parks have great potential for conserving more endangered plant species, not only for trees but also for shrubs and herbs. To date, C. chinensis has been introduced to botanical gardens in 14 cities (Beijing, Xi’an, Chengdu, Kunming, Chongqing, Changsha, Jiujiang, Wuhan, Hefei, Nanjing, Shanghai, Ningbo, Hangzhou, and

that C. chinensis lives in sparse forests with canopy densities of 20%–60%, we determined that 26.5% block-shaped green spaces are suitable for C. chinensis in Hangzhou (Table 3). Sparse forests can be potential habitats for this species because they meet the ecological niche requirements of this species, both in terms of light and wind requirements. Furthermore, Hangzhou city is located within native distribution areas of C. chinensis; thus, climate will not be a limiting factor (Fan et al., 2016). Fortunately, the rapid expansion of urban green spaces (Fuller and Gaston, 2009) can provide additional habitats for the conservation of endangered plants (Li et al., 2006; Kümmerling and Müller, 2012). Notably, the increase in park green spaces area is also higher than that of urban green spaces (Fig. 6). Diverse habitats in

Table 2 Photosynthetic parameters and functional traits of Calycanthus chinensis and the two other species. Species Chl a/b ratio Specific leaf area (cm2 g−1) Area per leaf (cm2) Leaf number per branch Leaf area per branch (cm2)

C. chinensis

Chimonanthus praecox a

b

1.75 ± 0.15 160.68 ± 11.56b 33.42 ± 5.27b 35 ± 6b 780.59 ± 56.46a

2.58 ± 0.13 237.92 ± 21.24a 152.38 ± 14.35a 9 ± 1c 658.59 ± 35.72b

Notes: Values are means ± SE. The different letters denote significant differences among species. 6

Chimonanthus salicifolius 1.20 ± 0.16b 177.93 ± 13.95b 12.65 ± 2.17c 79 ± 10a 751.42 ± 55.68a

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Fig. 5. The area per leaf and specific leaf area (means ± SE) of Calycanthus chinensis and two other species (Chimonanthus praecox and Chimonanthus salicifolius) (a) and an illustration of the large and thin leaves of Calycanthus chinensis that are easily damaged by wind (b) and photos of leaves of Calycanthus chinensis that are damaged by wind in Hangzhou Botanical Garden (c) and in the field (d).

endangered plants to cities also improves the evenness of the distribution of endangered species at a large scale, thus improving the regional plant diversity (Meffin et al., 2010), which is γ-diversity. This study also showed that compared with the urban edge, the green spaces close to the urban centre have higher tree diversity (Table 4). This result was consistent with the richness pattern across the urban-rural gradient conducted in other studies (Hope, 2003; Walker et al., 2009). High biodiversity in urban areas demonstrates that people are willing to spend more money to improve the quality of urban green spaces to ensure higher ecosystem cultural services (Chang et al., 2017), although in comparison to other areas, these places have higher land prices. This scenario may be because higher-income urban areas support more species (Hope, 2003). Introducing C. chinensis (endangered species) to urban green spaces coincides with people’s desire for a more diverse plant community in urban green spaces. People’s preference for more species provides an opportunity for introducing endangered species to urban areas. Furthermore, introducing new species will also fill vacant niches (Dlugosch et al., 2015) that often occur in artificial urban green spaces, thus optimizing the structure and improving the quality of green spaces. Increasing biodiversity in urban green spaces can improve the recreational values of ecosystem services (Palliwoda et al., 2017). It can also contribute to social and cultural goals, such as improving landscape aesthetics and educational value (MA, 2005). The introduction of endemic endangered species, such as C. chinensis, could instil public

Taizhou) in China. In addition, C. chinensis has been spread successfully to botanical gardens in many countries in Europe (France), North America (Canada and USA), and East Asia (Japan) from Hangzhou Botanical Garden by means of seeds. Although these C. chinensis individuals are only limited to botanical gardens now, at least it indicated C. chinensis could be introduced to areas outside its natural range. Some researchers believe that introducing a species outside its natural distribution areas can provide external “ecological memory” (i.e., population sources) for habitat recolonization (Bengtsson et al., 2003; Hansen and Defries, 2007; Xun et al., 2017) and provide genetic diversity (Groffman et al., 2014). To date, there have been no individuals of C. chinensis in urban spaces. The introduction of this species would extend the conservation areas and establish new populations to increase its survival prospects. 3.3. Biodiversity and benefits of urban green spaces enhanced by introducing endangered species Biodiversity is typically measured by richness, difference and evenness. Introducing endangered species to urban green spaces can increase all three aspects. First, introducing an endangered species increases species richness locally (Ren et al., 2017). Second, endangered species are often phylogenetically different from common species in the same genus. Thus, such an introduction can also increase phylogenetic differences in urban areas (Groffman et al., 2014). Third, introducing

Table 3 Characteristics of the forest in block-shaped green spaces within parks in Hangzhou city. Idices

Dense forest

Middle dense forest

Sparse forest

Open field

Total

Canopy density (%) Light intensity under trees Frequency Potential habitats

80 - 100 Low 27% 1.9%

60 – 80 Low-moderate 39% 35.5%

20 - 60 Moderate 27% 26.5%

0 - 20 High 7% 0.1%

– – 100% 64.0%

7

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Fig. 6. Increasing trend in potential habitats (park green spaces) for Calycanthus chinensis compared with that of total urban green spaces and built-up areas. Relationship between green space area and park area from 2001 to 2013 (a). Different colours represent different cities (Hangzhou, Taizhou, Ningbo, Shaoxing, Zhoushan, and Huzhou) in southeastern China. Each point represents each year. Lines show the best-fit relations Y (N) =Y0 Nβ; illustration of the growth rates of urban built-up areas, green spaces, and parks (b). Data is from http://tjj.hangzhou.gov.cn.

choosing those urban green spaces with a low possibility of land-use change, such as park green spaces (Chang et al., 2012). Due to suitable growing conditions for trees in urban green spaces, a gradually increased canopy density has adverse effects on understory endangered plants such as C. chinensis. To maintain habitats for endangered species, appropriate management is necessary (Aronson et al., 2017). Considering that green spaces become dense as they grow, tree canopy density should be controlled through pruning as the forest grows and develops. Furthermore, these endangered species could be introduced back to natural reserves for habitat recolonization (Bengtsson et al., 2003; Hansen and DeFries, 2007; Xun et al., 2017). In addition, the conservation of endangered species in urban areas is a complementary approach to in situ conservation in nature reserves and cannot play the same role as nature reserves. Additionally, it is necessary to calculate the likelihood of species becoming naturalized or invasive species before introducing them in other cities (Richardson et al., 2009; Schwartz et al., 2012; McLean et al., 2017), especially areas outside the natural range of this species. Although it is an effective conservation measure to introduce an endangered plant species to urban areas, some researchers believe that the introduced species may become invasive (McLean et al., 2017). C. chinensis has been introduced and grown in Hangzhou Botanical Garden since 1964, and no self-propagating seedlings have been found to date. Therefore, we can conclude that the introduction of C. chinensis is associated with a low risk of becoming an invasive species.

Table 4 Two species diversity indices in the green spaces from the urban centre to the edge of Hangzhou city. Location

Shannon-Wiener index

Simpson index

Urban centre Middle Urban edge

2.41 2.28 2.15

0.86 0.83 0.81

pride in local youth and enhance the culture services of green spaces because endemic endangered or other endemic species have symbolic significance with psychological importance (Bolund and Hunhammar, 1999; Kümmerling and Müller, 2012). Our investigation showed that there were approximately 1 million tourists visiting the Hangzhou Botanical Garden each year, and many people were interested in C. chinensis. More than 3 thematic activities about endangered plants were held by Hangzhou Botanical Garden each year. Approximately 50 thousand students from primary schools and high schools are involved in these activities every year. The endangered plants in the exhibition area, including C. chinensis, have become one of the students' favourite attractions. As a successful introduced endangered species in Hangzhou Botanical Gardens, C. chinensis has increased cultural ecosystem services, especially in terms of ornamental and educational benefits. 3.4. Uncertainty of urban green spaces conserving endangered species Although urban green spaces offer sufficient potential habitats for endangered species conservation, there are also some uncertainties and even risks. One concern is genetic variations decline over time in isolated urban patches due to restricted gene flow (Johnson and MunshiSouth, 2017). One solution is to carry out artificial pollination from wild population and plant conspecifics from different areas for reducing within-population pollination and self-pollination and thus sustain high genetic variation (Oostermeijer et al., 2003). The other concern is appropriate pollinators in urban areas for introduced flowering plants. Although some studies have indicated that urban areas support substantial pollinators (Hall et al., 2017; Baldock et al., 2019), the pollination may be still a problem for some introduced endangered plant with special pollinators. Additionally, urban green spaces have substantial public disturbance (Palliwoda et al., 2017), which will cause negative effects on species, especially for K-strategy species with long life cycles and low fertility, such as C. chinensis. To mitigate these adverse effects, enhancing education for public and management protocols can shift human impacts on endangered species in urban green spaces from negative to positive (Aronson et al., 2017). Moreover, it is also beneficial for successfully introducing endangered species by

4. Conclusions Using C. chinensis as a case study, we provided an effective framework for introducing endangered plant species to urban green spaces. We also highlighted the role of rapidly expanding urban green spaces as a valuable complement to endangered plant conservation in addition to nature reserves. The introduction of endangered species into urban green spaces can also increase species diversity, enhance cultural services of green spaces and thus improve human well-being. However, clearly, introducing an endangered species to green spaces in parks is far from enough to protect a species. Future research should try to expand the introduction of endangered species to more types of green spaces in urban areas. Some studies focusing on tracking the population dynamics, as well as genetic diversity, of introduced species compared to that of the wild population, are also an important topic. We believe that the strategy of combining urban green space development and endangered species protection will contribute to biodiversity conservation and land-use planning in the future.

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Acknowledgements

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