NOTAS BREVES

Crassula ovata, a new alien plant for mainland China

Z.-Q. WANG (王志强)1, D. GUILLOT2 & J. LÓPEZ-PUJOL3

1 Key Laboratory for Bio-resources and Eco-environment, College of Life Sciences, Sichuan University, CN-610065 Chengdu, Sichuan, People’s Republic of China

2 Botanic Garden, University of Valencia, c. Quart, 82, ES-46008 Valencia, Spain

3 Botanic Institute of Barcelona (IBB-CSIC-ICUB), pg. del Migdia, s/n, ES-08038 Barcelona, Spain

E-mail: J. López-Pujol jlopez@ibb.csic.es

Editor: A. Susanna

ABSTRACT
Crassula ovata, a new alien plant for mainland China.— Crassula ovata, the jade plant, is reported for the first time from mainland China. Two small populations have been discovered in the downtown of the city of Chengdu (Sichuan Province, western China).
KEYWORDS: alien species; casual; China; Crassula ovata; Sichuan.

Crassula ovata, una nueva especie alóctona para China continental

RESUMEN
Crassula ovata, una nueva especie alóctona para China continental.— Se reporta por primera vez la presencia de Crassula ovata, o planta de jade, en China continental. Se han descubierto dos pequeñas poblaciones en el centro de la ciudad de Chengdu (provincia de Sichuan, oeste de China).
PALABRAS CLAVE: especies alóctonas; Crassula ovata; China; Sichuan; subespontánea.

摘要
中国大陆发现一种新的外来物种;翡翠木。— 翡翠木也称之为厚叶景天,中国大陆地区第一次报道了该物种属于外来物种,并在位于中国西部四川省成都市的市区中发现了该物种两个小居群。
关键词:外来物种;常见物种;翡翠木;中国;四川。

Recibido: 03/09/2015 / Aceptado: 22/10/2015

Cómo citar este artículo / Citation: Wang, Z.-Q., Guillot, D. & López-Pujol, J. 2015. Crassula ovata, a new alien plant for mainland China. Collectanea Botanica 34: e009. doi: http://dx.doi.org/10.3989/collectbot.2015.v34.009

Copyright: © 2015 Institut Botànic de Barcelona (CSIC). Este es un artículo de acceso abierto distribuido bajo los términos de la licencia Creative Commons Attribution-Non Commercial (by-nc) Spain 3.0. This is an open-access article distributed under the terms of the Creative Commons Attribution-Non Commercial (by-nc) Spain 3.0 License.

CONTENIDOS

ABSTRACT
RESUMEN
摘要
ACKNOWLEDGEMENTS
REFERENCES

The genus Crassula comprises nearly 200 species mainly distributed in southern Africa (its center of distribution), with some species distributed in other parts of Africa or other parts of the world (Jaarsveld, 2003Jaarsveld, E. van 2003. Crassula. In: Eggli, U. (Ed.), Illustrated handbook of succulent plants: Crassulaceae. Springer-Verlag, Berlin: 32–84. ). Perhaps the best known species within the genus is Crassula ovata (Mill.) Druce, the jade plant, which is cultivated everywhere as an ornamental plant. According to Jaarsveld (2003Jaarsveld, E. van 2003. Crassula. In: Eggli, U. (Ed.), Illustrated handbook of succulent plants: Crassulaceae. Springer-Verlag, Berlin: 32–84. ), Crassula ovata is native to South Africa (Eastern Cape and KwaZulu-Natal provinces). However, it also occurs in other regions of southern Africa, such as Mozambique and Swaziland, where it is also probably native (Invasive Species Compendium, 2015Invasive Species Compendium 2015. Crassula ovata (jade plant) – datasheet. Centre for Agriculture and Biosciences International, Wallingford. Retrieved August 25, 2015, from http://www.cabi.org/isc/datasheet/113574). It is present in the wild (casual or naturalized) in other territories of Africa (Canary Islands, Madeira), Europe (Spain, Italy), America (California in the United States, Mexico), and Oceania (Hawaii, Australia, New Zealand) (DAISIE, 2015DAISIE (Delivering Alien Invasive Species Inventories for Europe) 2015. Species factsheet: Crassula ovata. DAISIE European Invasive Alien Species Gateway. Retrieved August 16, 2015, from http://www.europe-aliens.org/speciesFactsheet.do?speciesId=8750#; GBIF, 2015GBIF (Global Biodiversity Information Facility) 2015. Crassula ovata (Mill.) Druce. GBIF Secretariat, Copenhagen. Retrieved August 27, 2015, from http://www.gbif.org/species/5362063; Invasive Species Compendium, 2015Invasive Species Compendium 2015. Crassula ovata (jade plant) – datasheet. Centre for Agriculture and Biosciences International, Wallingford. Retrieved August 25, 2015, from http://www.cabi.org/isc/datasheet/113574), likely as the result of its use as ornamental; C. ovata has been grown beyond its native range as an ornamental (usually under the synonym Crassula portulacea Lam.) since the eighteenth century due to its beauty, easy propagation (from stem of leaf cuttings), and beliefs (it brings “good financial luck”; Malan & Notten, 2005Malan, C. & Notten, A. 2005. Crassula ovata (Miller) Druce. South African National Biodiversity Institute, Silverton. Retrieved August 26, 2015, from http://www.plantzafrica.com/plantcd/crassovat.htm). Despite its capability to spread, it is not a serious weed, with no records of significant invasions (Invasive Species Compendium, 2015Invasive Species Compendium 2015. Crassula ovata (jade plant) – datasheet. Centre for Agriculture and Biosciences International, Wallingford. Retrieved August 25, 2015, from http://www.cabi.org/isc/datasheet/113574) except for some areas (e.g. in coastal areas of Valencia, Spain; Ferrer & Donat, 2011Ferrer, F. & Donat, P. M. 2011. Invasive plants in the coastal vegetal communities in Valencia (Spain). Notulae Botanicae Horti Agrobotanici Cluj-Napoca 39: 09–17.).

According to all major regional taxonomic works (Flora of China, Flora Reipublicae Popularis Sinicae, Flora of Taiwan, Flora of Hong Kong) not only Crassula ovata but the whole genus is absent in China (including Taiwan). Moreover, C. ovata is not included in any of the lists or compendiums on alien plants in China published during the last decade (e.g. Wu et al., 2004Wu, S.-H., Hsieh, C.-F. & Rejmánek, M. 2004. Catalogue of the naturalized flora of Taiwan. Taiwania 49: 16–31. http://dx.doi.org/10.6165/tai.2004.49(1).16, 2010aWu, S.-H., Sun, H.-T., Teng, Y.-C., Rejmánek, M., Chaw, S.-M., Yang, T.-Y. A. & Hsieh, C.-F. 2010a. Patterns of plant invasions in China: taxonomic, biogeographic, climatic approaches and anthropogenic effects. Biological Invasions 12: 2179–2206. http://dx.doi.org/10.1007/s10530-009-9620-3, 2010bWu S.-H., Yang, T. Y. A., Teng, Y.-C., Chang C.-Y., Yang K.-C. & Hsieh, C.-F. 2010b. Insights of the latest naturalized flora of Taiwan: Change in the past eight years. Taiwania 55: 139–159. http://dx.doi.org/10.6165/tai.2010.55(2).139; Lin et al., 2007Lin, W., Zhou, G., Cheng, X. & Xu, R. 2007. Fast economic development accelerates biological invasions in China. PLoS One 2: e1208. http://dx.doi.org/10.1371/journal.pone.0001208; Weber et al., 2008Weber, E., Sun, S. G. & Li, B. 2008. Invasive alien plants in China: diversity and ecological insights. Biological Invasions 10: 1411–1429. http://dx.doi.org/10.1007/s10530-008-9216-3; Fang & Wan, 2009Fang, J. & Wan, F. 2009. Invasive species and their impacts on endemic ecosystems in China. In: Kohli, R. K., Jose, S., Singh, H. P. & Batish, D. R. (Eds.), Invasive plants and forest ecosystems. CRC Press, Boca Raton: 157–175.; Jiang et al., 2011Jiang, H., Fan, Q., Li, J.-T., Shi, S., Li, S.-P., Liao, W.-B. & Shu, W.-S. 2011. Naturalization of alien plants in China. Biodiversity and Conservation 20: 1545–1556. http://dx.doi.org/10.1007/s10531-011-0044-x; Xu et al., 2012Xu, H., Qiang, S., Genovesi, P. et al. 2012. An inventory of invasive alien species in China. NeoBiota 15: 1–26. http://dx.doi.org/10.3897/neobiota.15.3575; Axmacher & Sang, 2013Axmacher, J. C. & Sang, W. 2013. Plant invasions in China – challenges and changes. PLoS One 8: e64173. http://dx.doi.org/10.1371/journal.pone.0064173; Yan et al., 2014Yan, X., Liu, Q., Shou, H. et al. 2014. 中国外来入侵植物的等级划分与地理分布格局分析 [The categorization and analysis on the geographic distribution patterns of Chinese alien invasive plants]. Biodiversity Science 22: 667–676 [in Chinese]. http://dx.doi.org/10.3724/SP.J.1003.2014.14069). Wild occurrences of the jade plant are also not reported in any of the major databases, information systems, and citizen science projects focused on China, including Global Biodiversity Information Facility (GBIF; www.gbif.org/), Chinese Virtual Herbarium (CVH; www.cvh.ac.cn), Taiwan Biodiversity Information Facility (TaiBIF; www.taibif.tw), iNaturalist (www.inaturalist.org), Chinese Field Herbarium (CFH; www.cfh.ac.cn), and Plant Photo Bank of China (PPBC; www.plantphoto.cn). However, C. ovata is included in the Check List of Hong Kong Plants (Hong Kong Herbarium, 2004Hong Kong Herbarium 2004. Check list of Hong Kong plants 2004. Agriculture, Fisheries and Conservation Department (the Government of Hong Kong Special Administrative Region), Hong Kong. ) under one of its synonyms (Crassula argentea Thunb.).

In the course of a field investigation in tropical and subtropical areas of China, we observed two populations of C. ovata in the city of Chengdu (Sichuan Province, SW China). Thus, these populations apparently represent new records for mainland China. The identification of C. ovata is straightforward, as the species is very characteristic even in the absence of flowers (by its jade-green obovate leaves of 3–9 cm long, often with reddish acute margins; Jaarsveld, 2003Jaarsveld, E. van 2003. Crassula. In: Eggli, U. (Ed.), Illustrated handbook of succulent plants: Crassulaceae. Springer-Verlag, Berlin: 32–84. ). Both populations are located in the downtown; one is composed by a small colony of a dozen vegetative individuals on a small roof at a building façade (accompanied by Kalanchoe daigremontiana Raym.-Hamet & H. Perrier, also a common invader; Fig. 1) in Wuhou District (near the Sichuan University campus); the second one consisted of just 4–5 vegetative individuals (stems) also on a small roof at a building façade in Qingyang District (near Wenshu Temple; Fig. 1). Since we observed Crassula ovata cultivated as a pot plant in several places of Chengdu, these wild populations are likely escapes from private gardens. Crassula ovata should be, thus, regarded as casual in China, but paying special attention to its potential for naturalization. We believe that there is a considerable risk of naturalization, given that the plant is cultivated in many places of China (the PPBC hosts several images of C. ovata planted in pots in at least 13 provinces), its ease of propagation (even single leaves can produce roots and grow into new plants; Invasive Species Compendium, 2015Invasive Species Compendium 2015. Crassula ovata (jade plant) – datasheet. Centre for Agriculture and Biosciences International, Wallingford. Retrieved August 25, 2015, from http://www.cabi.org/isc/datasheet/113574), and its tolerance to a wide range of temperature and humidity (even tolerating light frost; Mahr, 2010Mahr, S. 2010. Jade plant. University of Wisconsin-Extension Master Gardener Program, Madison. Retrieved August 26, 2015, from http://wimastergardener.org/?q=JadePlant).

Figure 1. Observed populations of Crassula ovata from Chengdu (Sichuan, China): left, from Wuhou District (note that there is an individual of Kalanchoe daigremontiana on the right); right, from Qingyang District (Photographs: J. López-Pujol).

Imagen

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The recording of a new alien species for the Chinese flora such as C. ovata is not a rare event and should be included within the process of acceleration of plant invasions that is affecting the country (mainly as consequence of the economic boom; e.g. Ding et al., 2008Ding, J., Mack, R. N., Lu, P., Ren, M. & Huang, H. 2008. China’s booming economy is sparking and accelerating biological invasions. Bioscience 58: 317–324. http://dx.doi.org/10.1641/B580407). The lists of invasive and naturalized plant species have increased several-fold in just two decades (Jiang et al., 2011Jiang, H., Fan, Q., Li, J.-T., Shi, S., Li, S.-P., Liao, W.-B. & Shu, W.-S. 2011. Naturalization of alien plants in China. Biodiversity and Conservation 20: 1545–1556. http://dx.doi.org/10.1007/s10531-011-0044-x; Axmacher & Sang, 2013Axmacher, J. C. & Sang, W. 2013. Plant invasions in China – challenges and changes. PLoS One 8: e64173. http://dx.doi.org/10.1371/journal.pone.0064173) and such exponential growth is expected to continue in the future (Xu et al., 2012Xu, H., Qiang, S., Genovesi, P. et al. 2012. An inventory of invasive alien species in China. NeoBiota 15: 1–26. http://dx.doi.org/10.3897/neobiota.15.3575; Kleunen et al., 2015Kleunen, M. van, Dawson, W., Essl, F. et al. 2015. Global exchange and accumulation of non-native plants. Nature 525: 100–103. http://dx.doi.org/10.1038/nature14910). A large part of the naturalized plant species in China (over 40%) have been introduced intentionally as ornamentals (Wu et al., 2010aWu, S.-H., Sun, H.-T., Teng, Y.-C., Rejmánek, M., Chaw, S.-M., Yang, T.-Y. A. & Hsieh, C.-F. 2010a. Patterns of plant invasions in China: taxonomic, biogeographic, climatic approaches and anthropogenic effects. Biological Invasions 12: 2179–2206. http://dx.doi.org/10.1007/s10530-009-9620-3), and the latest tendencies in gardening and landscaping in China are clearly biased towards alien species. In Beijing, for example, half of the plant species grown in urban green spaces are of alien origin (Wang et al., 2012Wang, H.-F., MacGregor-Fors, I. & López-Pujol, J. 2012. Warm-temperate, immense, and sprawling: plant diversity drivers in urban Beijing, China. Plant Ecology 213: 967–992. http://dx.doi.org/10.1007/s11258-012-0058-9), and many invasives were involved in the “greening” of the city for the 2008 Olympic Games (Wang et al., 2011Wang H.-F., López-Pujol, J., Meyerson, L. A., Qiu, J.-X., Wang X.-K. & Ouyang, Z.-Y. 2011. Biological invasions in rapidly urbanizing areas: a case study of Beijing, China. Biodiversity and Conservation 20: 2483–2509. http://dx.doi.org/10.1007/s10531-011-9999-x).

Voucher specimens: China, Sichuan: Chengdu, Wuhou District, 30.64º N, 104.08º E, 495 m, on a building façade, growing together with Kalanchoe daigremontiana, 27.08.2015, Z.-Q. Wang (SZ-00356563, SZ-00356564); Chengdu, Qingyang District, 30.67º N, 104.07º E, 505 m, on a building façade, 28.05.2015, J. López-Pujol (BC, photo voucher; Fig. 1).

ACKKNOWLEDGEMENTSTop

Z.-Q. Wang has benefited from a postdoctoral fund of Sichuan University.

REFERENCESTop

1. Axmacher, J. C. & Sang, W. 2013. Plant invasions in China – challenges and changes. PLoS One 8: e64173. http://dx.doi.org/10.1371/journal.pone.0064173
2. DAISIE (Delivering Alien Invasive Species Inventories for Europe) 2015. Species factsheet: Crassula ovata. DAISIE European Invasive Alien Species Gateway. Retrieved August 16, 2015, from http://www.europe-aliens.org/speciesFactsheet.do?speciesId=8750#
3. Ding, J., Mack, R. N., Lu, P., Ren, M. & Huang, H. 2008. China’s booming economy is sparking and accelerating biological invasions. Bioscience 58: 317–324. http://dx.doi.org/10.1641/B580407
4. Fang, J. & Wan, F. 2009. Invasive species and their impacts on endemic ecosystems in China. In: Kohli, R. K., Jose, S., Singh, H. P. & Batish, D. R. (Eds.), Invasive plants and forest ecosystems. CRC Press, Boca Raton: 157–175.
5. Ferrer, F. & Donat, P. M. 2011. Invasive plants in the coastal vegetal communities in Valencia (Spain). Notulae Botanicae Horti Agrobotanici Cluj-Napoca 39: 09–17.
6. GBIF (Global Biodiversity Information Facility) 2015. Crassula ovata (Mill.) Druce. GBIF Secretariat, Copenhagen. Retrieved August 27, 2015, from http://www.gbif.org/species/5362063
7. Hong Kong Herbarium 2004. Check list of Hong Kong plants 2004. Agriculture, Fisheries and Conservation Department (the Government of Hong Kong Special Administrative Region), Hong Kong.
8. Invasive Species Compendium 2015. Crassula ovata (jade plant) – datasheet. Centre for Agriculture and Biosciences International, Wallingford. Retrieved August 25, 2015, from http://www.cabi.org/isc/datasheet/113574
9. Jaarsveld, E. van 2003. Crassula. In: Eggli, U. (Ed.), Illustrated handbook of succulent plants: Crassulaceae. Springer-Verlag, Berlin: 32–84.
10. Jiang, H., Fan, Q., Li, J.-T., Shi, S., Li, S.-P., Liao, W.-B. & Shu, W.-S. 2011. Naturalization of alien plants in China. Biodiversity and Conservation 20: 1545–1556. http://dx.doi.org/10.1007/s10531-011-0044-x
11. Kleunen, M. van, Dawson, W., Essl, F. et al. 2015. Global exchange and accumulation of non-native plants. Nature 525: 100–103. http://dx.doi.org/10.1038/nature14910
12. Lin, W., Zhou, G., Cheng, X. & Xu, R. 2007. Fast economic development accelerates biological invasions in China. PLoS One 2: e1208. http://dx.doi.org/10.1371/journal.pone.0001208
13. Mahr, S. 2010. Jade plant. University of Wisconsin-Extension Master Gardener Program, Madison. Retrieved August 26, 2015, from http://wimastergardener.org/?q=JadePlant
14. Malan, C. & Notten, A. 2005. Crassula ovata (Miller) Druce. South African National Biodiversity Institute, Silverton. Retrieved August 26, 2015, from http://www.plantzafrica.com/plantcd/crassovat.htm
15. Wang H.-F., López-Pujol, J., Meyerson, L. A., Qiu, J.-X., Wang X.-K. & Ouyang, Z.-Y. 2011. Biological invasions in rapidly urbanizing areas: a case study of Beijing, China. Biodiversity and Conservation 20: 2483–2509. http://dx.doi.org/10.1007/s10531-011-9999-x
16. Wang, H.-F., MacGregor-Fors, I. & López-Pujol, J. 2012. Warm-temperate, immense, and sprawling: plant diversity drivers in urban Beijing, China. Plant Ecology 213: 967–992. http://dx.doi.org/10.1007/s11258-012-0058-9
17. Weber, E., Sun, S. G. & Li, B. 2008. Invasive alien plants in China: diversity and ecological insights. Biological Invasions 10: 1411–1429. http://dx.doi.org/10.1007/s10530-008-9216-3
18. Wu, S.-H., Hsieh, C.-F. & Rejmánek, M. 2004. Catalogue of the naturalized flora of Taiwan. Taiwania 49: 16–31. http://dx.doi.org/10.6165/tai.2004.49(1).16
19. Wu, S.-H., Sun, H.-T., Teng, Y.-C., Rejmánek, M., Chaw, S.-M., Yang, T.-Y. A. & Hsieh, C.-F. 2010a. Patterns of plant invasions in China: taxonomic, biogeographic, climatic approaches and anthropogenic effects. Biological Invasions 12: 2179–2206. http://dx.doi.org/10.1007/s10530-009-9620-3
20. Wu S.-H., Yang, T. Y. A., Teng, Y.-C., Chang C.-Y., Yang K.-C. & Hsieh, C.-F. 2010b. Insights of the latest naturalized flora of Taiwan: Change in the past eight years. Taiwania 55: 139–159. http://dx.doi.org/10.6165/tai.2010.55(2).139
21. Xu, H., Qiang, S., Genovesi, P. et al. 2012. An inventory of invasive alien species in China. NeoBiota 15: 1–26. http://dx.doi.org/10.3897/neobiota.15.3575
22. Yan, X., Liu, Q., Shou, H. et al. 2014. 中国外来入侵植物的等级划分与地理分布格局分析 [The categorization and analysis on the geographic distribution patterns of Chinese alien invasive plants]. Biodiversity Science 22: 667–676 [in Chinese]. http://dx.doi.org/10.3724/SP.J.1003.2014.14069