Biodiversity Science ›› 2017, Vol. 25 ›› Issue (12): 1285-1294.doi: 10.17520/biods.2017096

• Special Feature: Biological Invasion • Previous Article     Next Article

Biological control opportunities of ragweed are predicted to decrease with climate change in East Asia

Yan Sun1,*(), Zhongshi Zhou2, Rui Wang2, Heinz Müller-Schärer3   

  1. 1 Plant Evolutionary Ecology, University of Tübingen, 72076 Tübingen, Germany ;
    2 State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, China
    3 Department of Biology/ Ecology & Evolution, University of Fribourg, 1700 Fribourg, Switzerland;
  • Received:2017-03-24 Accepted:2017-06-10 Online:2017-12-10
  • Sun Yan

The control of invasive alien plants (IAP) that jeopardize our ecosystems and economy constitutes a significant challenge for natural resource management. Classical biological control referring to the introduction of specialist antagonists from the native range has proven to be a highly cost-effective management tool against IAP. A critical issue in biological control research is to guide informed decision-making on the potential spread and distribution and thus impact of biological control candidates, especially under climate change. Here we propose a biogeographic modeling approach to predict the cover of the suitable area of a plant invader in East Asia (EA) by two biological control agents and their combinations. Our study system is Ambrosia artemisiifolia, native to North America and invasive worldwide, and two North American biological control agents, Ophraella communa and Epiblema strenuana that were accidentally and deliberately introduced into East Asia (EA) in the late 20th century, respectively. Specifically, we ask: (1) what percentage of the suitable A. artemisiifolia area is also suitable for the two agents in EA, and (2) which part of the suitable A. artemisiifolia area in EA is likely to remain uncovered by these two agents, both under current and future climatic scenarios; and (3) which particular biotypes would be needed to fill in the yet uncovered part of the suitable A. artemisiifolia range in East Asia? For this, we simultaneously modelled the species distributions based on worldwide occurrences and important bioclimatic variables for the target invasive plant and its two biological control agents. Ordination techniques were used to explore climatic constraints of each species and to perform niche overlap and similarity tests with A. artemisiifolia between its native North American and introduced EA range. Our results show that O. communa has a larger overlap with the geographic range of A. artemisiifolia than E. strenuana, both under current (40.3% vs. 21.6% for O. communa and E. strenuana, respectively) and future climatic scenarios (29.8% vs. 20.3% for O. communa and E. strenuana, respectively). Importantly, climate change is expected to reduce the total geographic overlap of A. artemisiifolia by the two agents combined (42.9% vs. 29.8% for current and future climate conditions, respectively), with a higher reduction by O. communa than by E. strenuana. Our analyses also identified for which abiotic conditions to select in order to develop climatically adapted strains for particular regions, where A. artemisiifolia is presently unlikely to be covered.

Key words: biological control, biological invasions, Epiblema strenuana, niche overlap, Ophraella communa, species distribution

Table 1

AUC power of all species using four models under current and future climate scenarios showing acceptable AUC scores"

Ambrosia artemisiifolia Ophraella communa Epiblema strenuana
当前气候背景 Current climate scenario
一般线性模型 GLM 0.88±0.002 0.88±0.004 0.84±0.01
广义助推模型 GBM 0.89±0.002 0.90±0.003 0.89±0.006
随机森林模型 RF 0.89±0.003 0.91±0.003 0.89±0.006
最大熵模型MaxEnt 0.87±0.003 0.83±0.004 0.83±0.009

未来气候背景: HD-26 Future climate scenario: HD-26
一般线性模型 GLM 0.87±0.003 0.87±0.002 0.83±0.01
广义助推模型 GBM 0.89±0.002 0.90±0.002 0.90±0.006
随机森林模型 RF 0.90±0.002 0.91±0.002 0.91±0.006
最大熵模型MaxEnt 0.86±0.003 0.83±0.003 0.80±0.01

未来气候背景: HD-85 Future climate scenario: HD-85
一般线性模型 GLM 0.88±0.003 0.88±0.002 0.84±0.008
广义助推模型 GBM 0.90±0.003 0.92±0.001 0.86±0.008
随机森林模型 RF 0.89±0.003 0.92±0.001 0.86±0.009
最大熵模型MaxEnt 0.88±0.003 0.84±0.003 0.78±0.01

未来气候背景: IP-26 Future climate scenario: IP-26
一般线性模型 GLM 0.89±0.003 0.87±0.002 0.87±0.01
广义助推模型 GBM 0.90±0.002 0.90±0.002 0.91±0.008
随机森林模型 RF 0.91±0.002 0.91±0.001 0.91±0.008
最大熵模型MaxEnt 0.89±0.003 0.85±0.002 0.82±0.009

未来气候背景: IP-85 Future climate scenario: IP-85
一般线性模型 GLM 0.87±0.003 0.87±0.002 0.88±0.008
广义助推模型 GBM 0.89±0.003 0.90±0.002 0.91±0.006
随机森林模型 RF 0.91±0.003 0.91±0.002 0.91±0.006
最大熵模型MaxEnt 0.87±0.003 0.84±0.003 0.88±0.008

Fig. 1

Geographical predictions of Ambrosia artemisiifolia and two biological control insects for East Asia, under present and future climatic scenarios. The climatic suitability indicates the optimal threshold of the percentage of models predicting each species. Dark green in all figures, A. artemisiifolia; under current climatic conditions: (A) Red, Ophraella communa; sienna, overlap 40.3%; (B) Blue, Epiblema strenuana; sienna, overlap 21.6%; under future climatic scenarios: (C) Red, Ophraella communa; sienna, overlap 29.8%; (D) Blue, Epiblema strenuana; sienna, overlap 20.3%. Models calibrated in East Asia only."

Fig. 2

Niche of Ambrosia artemisiifolia in climatic space using principal component analysis (PCA-env). Panels (A) and (B) represent the niche of the species along the two first axes of the PCA for the native North American (NA) and introduced East Asian (EA) range, respectively. Gray shading shows the density of the occurrences of the species by the cell. The solid contour lines illustrate 100% of the available environment, and dashed lines indicate the 50% of the most common background environment. Yellow circles in (A) and (B) give the occurrences of two insect species in NA and in EA. The contribution of the climatic variables of the two axes of the PCA and the percentage of inertia explained by the two axes is given in (C). Histograms (D-F) show the observed niche overlap between the two ranges (bars and a diamond) and simulated niche overlaps (gray bars) on which tests of niche equivalency (D), niche similarity of EA and NA (E), and niche similarity of NA and EA (F) are calculated from 100 iterations, with the significance level of the tests."

[1] Araújo MB, New M (2007) Ensemble forecasting of species distributions. Trends in Ecology & Evolution, 22, 42-47.
[2] Barriopedro D, Fischer EM, Luterbacher J, Trigo RM, García-Herrera R (2011) The hot summer of 2010: redrawing the temperature record map of Europe. Science, 332, 220-224.
[3] Björkman C, Niemelä P (2015) Climate Change and Insect Pests. CABI, Oxfordshire, UK.
[4] Broennimann O, Fitzpatrick MC, Pearman PB, Petitpierre B, Pellissier L, Yoccoz NG, Thuiller W, Fortin MJ, Randin C, Zimmermann NE (2012) Measuring ecological niche overlap from occurrence and spatial environmental data. Global Ecology and Biogeography, 21, 481-497.
[5] Broennimann O, Petitpierre B, Randin C, Engler R, Breiner F, Manuela D, Pellissier L, Pottier J, Pio D, Mateo RG (2014) Package ‘ecospat’. .
[6] Cola VD, Broennimann O, Petitpierre B, Breiner FT, D’Amen M, Randin C, Engler R, Pottier J, Pio D, Dubuis A (2016) ecospat: an R package to support spatial analyses and modeling of species niches and distributions. Ecography, 40, 774-787.
[7] Essl F, Biró K, Brandes D, Broennimann O, Bullock JM, Chapman DS, Chauvel B, Dullinger S, Fumanal B, Guisan A (2015) Biological flora of the British Isles: Ambrosia artemisiifolia. Journal of Ecology, 103, 1069-1098.
[8] Fukano Y, Doi H (2013) Population abundance and host use pattern of Ophraella communa (Coleoptera: Chrysomelidae) in its native and introduced range. Biocontrol Science and Technology, 23, 595-601.
[9] Fukano Y, Yahara T (2012) Changes in defense of an alien plant Ambrosia artemisiifolia before and after the invasion of a native specialist enemy Ophraella communa. PLoS ONE, 7, e49114.
[10] Futuyma DJ, McCafferty SS (1990) Phylogeny and the evolution of host plant associations in the leaf beetle genus Ophraella (Coleoptera, Chrysomelidae). Evolution, 44, 1885-1913.
[11] Gerber E, Schaffner U, Gassmann A, Hinz H, Seier M, Müller-Schärer H (2011) Prospects for biological control of Ambrosia artemisiifolia in Europe: learning from the past. Weed Research, 51, 559-573.
[12] Gillson L, Dawson TP, Jack S, McGeoch MA (2013) Accommodating climate change contingencies in conservation strategy. Trends in Ecology and Evolution, 28, 135-142.
[13] Giorgetta MA, Jungclaus J, Reick CH, Legutke S, Bader J, Böttinger M, Brovkin V, Crueger T, Esch M, Fieg K (2013) Climate and carbon cycle changes from 1850 to 2100 in MPI-ESM simulations for the Coupled Model Intercomparison Project phase 5. Journal of Advances in Modeling Earth Systems, 5, 572-597.
[14] Goolsby JA, De Barro PJ, Kirk AA, Sutherst RW, Canas L, Ciomperlik MA, Ellsworth PC, Gould JR, Hartley DM, Hoelmer KA (2005) Post-release evaluation of biological control of Bemisia tabaci biotype “B” in the USA and the development of predictive tools to guide introductions for other countries. Biological Control, 32, 70-77.
[15] Guisan A, Zimmermann NE (2000) Predictive habitat distribution models in ecology. Ecological Modelling, 135, 147-186.
[16] Hannah L, Midgley GF, Millar D (2002) Climate change— integrated conservation strategies. Global Ecology and Biogeography, 11, 485-495.
[17] Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A (2005) Very high resolution interpolated climate surfaces for global land areas. International Journal of Climatology, 25, 1965-1978.
[18] Hisauchi K (1950) Naturalized Plants. Kagakutosyo syuppan, Tokyo.
[19] Hoelmer K, Kirk A (2005) Selecting arthropod biological control agents against arthropod pests: Can the science be improved to decrease the risk of releasing ineffective agents? Biological Control, 34, 255-264.
[20] IPCC (2013) Climate change 2013: The Physical Science Basis.
[21] Kettenring KM, Adams CR (2011) Lessons learned from invas¬ive plant control experiments: a systematic review and meta-analysis. Journal of Applied Ecology, 48, 970-979.
[22] LeSage L (1986) A taxonomic monograph of the Nearctic galerucine genus Ophraella Wilcox (Coleoptera: Chryso¬m¬elidae). Memoirs of the Entomological Society of Canada, 118, 3-75.
[23] Li HK, Li M, Li D (1999) Ambrosia artemisiifolia and its biological control. World Agriculture, (8), 40-41. (in Chinese)
[李宏科, 李萌, 李丹 (1999) 豚草及其防治概况. 世界农业, (8), 40-41.]
[24] Ma J, Guo JY, Wan FH, Hu X, Wan FH, Li B, Guo J (2008) Biological control of Ambrosia artemisiifolia and A. trifida. In: Biological Invasions: Biological Control Theory and Practice, pp. 157-185. Science Press, Beijing. (in Chinese with English abstract)
[马骏, 郭建英, 万方浩 (2008) 普通豚草和三裂叶豚的生物防治, 见: 生物入侵: 生物防治篇(万方浩, 李保平, 郭建英主编), 157-185页. 科学出版社, 北京.]
[25] McFadyen RC (1992) Biological control against Parthenium weed in Australia. Crop Protection, 11, 400-407.
[26] Messenger P, van den Bosch R(1971) The adaptability of introduced biological control agents. In: Biological Control (ed. Huffaker CB), pp. 68-92. Springer, Boston.
[27] Moriya S, Shiyake S (2001) Spreading the distribution of an exotic ragweed beetle, Ophraella communa LeSage (Coleoptera: Chrysomelidae), in Japan. Japanese Journal of Entomology (New Series), 4, 99-102.
[28] Mukherjee A, Christman MC, Overholt WA, Cuda JP (2011) Prioritizing areas in the native range of hygrophila for surveys to collect biological control agents. Biological Control, 56, 254-262.
[29] Müller-Schärer H, Schaffner U (2008) Classical biological control: exploiting enemy escape to manage plant invasions. Biological Invasions, 10, 859-874.
[30] Palmer W, Goeden R (1991) The host range of Ophraella communa LeSage (Coleoptera: Chrysomelidae). The Coleopterists’ Bulletin, 45, 115-120.
[31] Pearce J, Ferrier S (2000) Evaluating the predictive performance of habitat models developed using logistic regression. Ecological Modelling, 133, 225-245.
[32] Peterson AT (2003) Predicting the geography of species’ invasions via ecological niche modeling. The Quarterly Review of Biology, 78, 419-433.
[33] Peterson AT (2011) Ecological niches and geographic distributions (MPB-49). Princeton University Press, New Jursey.
[34] Petitpierre B, Kueffer C, Broennimann O, Randin C, Daehler C, Guisan A (2012) Climatic niche shifts are rare among terrestrial plant invaders. Science, 335, 1344-1348.
[35] R Core Team (2016) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.2016) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. .
[36] Roderick GK, Hufbauer R, Navajas M (2012) Evolution and biological control. Evolutionary Applications, 5, 419-423.
[37] Schweiger O, Settele J, Kudrna O, Klotz S, Kühn I (2008) Climate change can cause spatial mismatch of trophically interacting species. Ecology, 89, 3472-3479.
[38] Seastedt TR (2015) Biological control of invasive plant species: a reassessment for the Anthropocene. New Phytologist, 205, 490-502.
[39] Sun Y, Brönnimann O, Roderick GK, Poltavsky A, Lommen STE, Müller-Schärer H (2017) Climatic suitability ranking of candidate biological control agents for weeds: a biogeographic approach for ragweed management in Europe under present and future climatic conditions. Ecosphere, 8, e01731.
[40] Tanaka K (2009) Genetic variation in flight activity of Ophraella communa (Coleoptera: Chrysomelidae): heritability estimated by artificial selection. Environmental Entomology, 38, 266-273.
[41] Tanaka K, Murata K, Matsuura A (2015) Rapid evolution of an introduced insect Ophraella communa LeSage in new environments: temporal changes and geographical differences in photoperiodic response. Entomological Science, 18, 104-112.
[42] Theoharides KA, Dukes JS (2007) Plant invasion across space and time: factors affecting nonindigenous species success during four stages of invasion. New Phytologist, 176, 256-273.
[43] Thuiller W, Georges D, Engler R (2013) Biomod2: ensemble platform for species distribution modeling. R package. .
[44] Vilà M, Espinar JL, Hejda M, Hulme PE, Jarošík V, Maron JL, Pergl J, Schaffner U, Sun Y, Pyšek P (2011) Ecological impacts of invasive alien plants: a meta-analysis of their effects on species, communities and ecosystems. Ecology Letters, 14, 702-708.
[45] Walker B, Steffen W (1997) An overview of the implications of global change for natural and managed terrestrial ecosystems. Conservation Ecology, 1, 2.
[46] Walther G-R, Roques A, Hulme PE, Sykes MT, Pyšek P, Kühn I, Zobel M, Bacher S, Botta-Dukát Z, Bugmann H (2009) Alien species in a warmer world: risks and opportunities. Trends in Ecology & Evolution, 24, 686-693.
[47] Wan FH, Liu WX, Ma J, Guo J (2005) Ambrosia artemisiifolia and A. trifida. In: Biology and Management of Invasive Alien Species in Agriculture and Forestry (eds Wan FH, Zheng XB, Guo JY), pp. 662-688. Science Press, Beijing. (in Chinese)
[万方浩, 刘万学, 马骏, 郭建英 (2005) 普通豚草和三裂叶豚草. 见: 重要农林外来入侵物种的生物学与控制(万方浩, 郑小波, 郭建英主编), 662-688页. 科学出版社, 北京.]
[48] Wan FH, Guan GQ, Wang R (1993) Ambrosia and Its Comprehensive Administration. Chinese Science and Technology Press, Beijing.
(in Chinese) [万方浩, 关广清, 王韧 (1993) 豚草及豚草综合治理. 中国科学技术出版社, 北京.]
[49] Winston RL, Schwarzländer M, Hinz HL, Day MD, Cock MJW, Julien MH (2014) Biological Control of Weeds: A World Catalogue of Agents and Their Target Weeds, 5th edn. USDA Forest Service, Forest Health Technology Enterprise Team, Virginia.
[50] Wisz MS, Hijmans R, Li J, Peterson AT, Graham C, Guisan A (2008) Effects of sample size on the performance of species distribution models. Diversity and Distributions, 14, 763-773.
[51] Yamazaki K, Imai C, Natuhara Y (2000) Rapid population growth and food-plant exploitation pattern in an exotic leaf beetle, Ophraella communa LeSage (Coleoptera: Chrysomelidae), in western Japan. Applied Entomology and Zoology, 35, 215-223.
[52] Zhou ZS, Chen HS, Zheng XW, Guo JY, Guo W, Li M, Luo M, Wan FH (2014) Control of the invasive weed Ambrosia artemisiifolia with Ophraella communa and Epiblema str¬enuana. Biocontrol Science and Technology, 24, 950-964.
[53] Zhou ZS, Guo JY, Chen HS, Wan FH (2010) Effects of temperature on survival, development, longevity, and fecundity of Ophraella communa (Coleoptera: Chrysomelidae), a potential biological control agent against Ambrosia artemisiifolia (Asterales: Asteraceae). Environmental Entomology, 39, 1021-1027.
[54] Zhou ZS, Guo JY, Michaud JP, Li M, Wan FH (2011a) Variation in cold hardiness among geographic populations of the ragweed beetle, Ophraella communa LeSage (Coleoptera: Chrysomelidae), a biological control agent of Ambrosia artemisiifolia L. (Asterales: Asteraceae), in China. Biological Invasions, 13, 659-667.
[55] Zhou ZS, Guo JY, Wan FH (2015) Review on management of Ambrosia artemisiifolia using natural enemy insects. Chinese Journal of Biological Control, 31, 657-665.
[56] Zhou ZS, Guo JY, Zheng XW, Luo M, Chen HS, Wan FH (2011b) Reevaluation of biosecurity of Ophraella communa against sunflower (Helianthus annuus). Biocontrol Science and Technology, 21, 1147-1160.
[57] Zhou ZS, Rasmann S, Li M, Guo JY, Chen HS, Wan FH (2013) Cold temperatures increase cold hardiness in the next generation Ophraella communa beetles. PLoS ONE, 8, e74760.
[1] Naiping Song, Xing Wang, Lin Chen, Yi Xue, Juan Chen, Jinming Sui, Lei Wang, Xinguo Yang. Co-existence mechanisms of plant species within “soil islands” habitat of desert steppe [J]. Biodiv Sci, 2018, 26(7): 667-677.
[2] Kaida Xu,Kaner Lu,Zhanhui Lu,Qian Dai. Ecological niche analysis of dominant shrimp species in the Jiushan Islands Marine Nature Reserve [J]. Biodiv Sci, 2018, 26(6): 601-610.
[3] Xuewei Gong,Guanghui Lü. Species diversity and dominant species’ niches of eremophyte communities of the Tugai forest in the Ebinur basin of Xinjiang, China [J]. Biodiv Sci, 2017, 25(1): 34-45.
[4] Chengye Hu,Yuyue Shui,Kuo Tian,Liang Li,Hulin Qin,Chuncao Zhang,Mengmeng Ji,Bonian Shui. Functional group classification and niche identification of major fish species in the Qixing Islands Marine Reserve, Zhejiang Province [J]. Biodiv Sci, 2016, 24(2): 175-184.
[5] Juncheng Lei,Sha Wang,Junwei Wang,Jun Wu. Potential effects of future climate change on suitable habitat of Muntiacus crinifrons, an endangered and endemic species in China [J]. Biodiv Sci, 2016, 24(12): 1390-1399.
[6] Guohong Liu,Bo Liu,Yujing Zhu,Jianmei Che,Cibin Ge,Mingxing Su,Jianyang Tang. Diversity of Bacillus-like species in Taiwan [J]. Biodiv Sci, 2016, 24(10): 1154-1163.
[7] Wen Wu,Yuehui Li,Yuanman Hu,Long Chen,Yue Li,Zeming Li,Zhiwen Nie,Tan Chen. Suitable winter habitat for Cervus elaphus on the southern slope of the Lesser Xing’an Mountains [J]. Biodiv Sci, 2016, 24(1): 20-29.
[8] Cheng Wen,Lei Gu,Hao Wang,Zhi Lü,Ruocheng Hu,Jia Zhong. GAP analysis on national nature reserves in China based on the distribution of endangered species [J]. Biodiv Sci, 2015, 23(5): 591-600.
[9] Shangbin Bai,Guomo Zhou,Yixiang Wang,Qianqian Liang,Juan Chen,Yanyan Cheng,Rui Shen. Plant species diversity and dynamics in forests invaded by Moso bamboo (Phyllostachys edulis) in Tianmu Mountain Nature Reserve [J]. Biodiv Sci, 2013, 21(3): 288-295.
[10] Ruiting Ju, Hui Li, Chengjen Shih, Bo Li. Progress of biological invasions research in China over the last decade [J]. Biodiv Sci, 2012, 20(5): 581-611.
[11] Ruiting Ju, Bo Li. A risk analysis system for alien species in urban green spaces and application to the 2010 Expo, Shanghai [J]. Biodiv Sci, 2012, 20(1): 12-23.
[12] Zhongping Tian, Li Zhuang, Jiangui Li, Moxiang Cheng. Interspecific and environmental relationships of woody plant species in wild fruit-tree forests on the north slope of Ili Valley [J]. Biodiv Sci, 2011, 19(3): 335-342.
[13] Wei Wang, Zhengrong Luo, Rongfei Zhou, Daming Xu, Jianguo Ai, Bingyang Ding. Habitat associations of woody plant species in Baishanzu subtropical broad-leaved evergreen forest [J]. Biodiv Sci, 2011, 19(2): 134-142.
[14] Yanbao Lei, Haifeng Xiao, Yulong Feng. Impacts of alien plant invasions on biodiversity and evolutionary responses of native species [J]. Biodiv Sci, 2010, 18(6): 622-630.
[15] Jian Liu, Junmin Li, Hua Yu, Weiming He, Feihai Yu, Weiguo Sang, Guofang Liu, Ming Dong. The relationship between functional traits and invasiveness of alien plants [J]. Biodiv Sci, 2010, 18(6): 569-576.
Full text



[1] Zhong Ye-cong. Five poems[J]. Chin Bull Bot, 1995, 12(专辑): 99 .
[2] Yang Dan-hui. The Effects of Heavy Metals on the Structure and Function of Photosynthetic Membranes in Higher Plants[J]. Chin Bull Bot, 1991, 8(03): 26 -29 .
[3] Tang Yancheng. A Short Guide to the International Code Botanical Nomenclature VIII[J]. Chin Bull Bot, 1985, 3(01): 59 -62 .
[4] JIANG Gao-Ming and HE Wei-Ming. A quick New Method for Determining Light Response Curves of Photosynthesis Under Field Light Conditions[J]. Chin Bull Bot, 1999, 16(06): 712 -718 .
[5] . [J]. Chin Bull Bot, 1994, 11(专辑): 66 .
[6] Zhou Guang-sheng Xing Xue-rong Wang Hui-min. Feedback of Forest on Climate[J]. Chin Bull Bot, 1995, 12(专辑2): 190 -194 .
[7] . [J]. Chin Bull Bot, 1994, 11(专辑): 74 .
[8] SHEN Jin-Xiong YI Bin FU Ting-Dong YANG Guang-Sheng. Overview on Mapping of Quantitative Traits for Plant[J]. Chin Bull Bot, 2003, 20(03): 257 -263 .
[9] Fan Guo-qiang and Tan Ke-hui. Inhibitory Effect of Non-induced Photoperiod on Plant Flowering[J]. Chin Bull Bot, 1997, 14(01): 8 -12 .
[10] Jing Wang;Ting Wang*;Yingjuan Su;Lin Sen;Bing Zhang;Yongxia Yang. Adaptive Evolution in the PHY-PAS1 Domain of PHYP in Gymnosperms[J]. Chin Bull Bot, 2009, 44(05): 608 -618 .