Phenotypic plasticity of Alternanthera philoxeroides in response to simulated daily warming: Introduced vs. native populations

doi:10.17520/biods.2020387

Abstract

Abstract:

Aims: The evolution of increased phenotypic plasticity hypothesis predicts that populations in the introduced range of an invasive species have evolved greater plasticity than populations in the native range. Studies of this hypothesis mostly focused on the plastic evolution of invasive plants to light, water, nutrients, neighboring plants, and natural enemies. However, there are relatively few studies focusing on the evolution of plasticity in plant growth and functional traits in response to warming. The few existing studies are concentrated in temperate regions and focus on growth-related traits, but relatively little attention has been paid to tropical regions and herbivory-related traits. To address this gap, we conducted an experiment with Alternanthera philoxeroides to study whether introduced and native populations of invasive plants differ in biomass, important functional traits and herbivory resistance in response to daily warming. Specifically, we addressed the following questions: (1) How do biomass, functional traits and herbivory damage of A. philoxeroides respond to simulated daily warming? (2) Do these responses differ between introduced and native populations of A. philoxeroides?

Methods: We conducted a field experiment in Zengcheng District (113.87° E, 23.33° N), Guangzhou City, Guangdong Province in which we grew eight populations of the invasive plantA. philoxeroides collected from both the introduced range (China) and the native range (Argentina) under ambient temperature and a condition of simulated daily warming of 2℃. After eight weeks of growth, we harvested all plants and measured the following variables: (1) biomass (i.e. total biomass and storage root biomass), (2) functional traits (i.e. branching intensity, specific stem length, root-to-shoot ratio and specific leaf area, and (3) herbivory damage (i.e. relative feeding area and stem-tip feeding proportion).

Results: Simulated daily warming of A. philoxeroides significantly reduced total biomass (-7.8%), storage root biomass (-12.8%), branching intensity (-11.6%) and stem-tip feeding proportion (-34.4%). The reduction in total biomass caused by the daily warming was greater in the introduced than in the native populations. Simulated daily warming reduced specific stem length and stem-tip feeding proportion of the introduced populations, while the native populations showed the opposite pattern. Regardless of simulated daily warming or not, storage root biomass (+31.5%), branch strength (+38.5%), specific stem length (+30.2%), root-to-shoot ratio (+24.5%) and specific leaf area (+20.0%) of the introduced populations were higher than those of the native populations, although stem-tip feeding proportion was lower (-35.8%).

Conclusion: These results indicate that simulated daily warming of 2℃ in tropical regions is a stressor for the invasive plant A. philoxeroides. Biomass of the introduced populations has stronger plasticity in response to simulated daily warming of 2℃ than that of the native populations. In response to simulated daily warming, plasticity of plant shape-related traits (specific stem length) and herbivory-related traits (stem-tip feeding proportion) of the introduced populations shows the opposite direction to that of the native populations. Given that the reduction in biomass reduction and increase in herbivory increase were greater in the introduced than the native populations, future temperature increases due to global climate change may not be beneficial to the abundance of invasive plant A. philoxeroides in the tropics.

Key words: warming, phenotypic plasticity, plant invasion, evolution

Heyan Huang, Zhengcai Zhu, Jihua Wu, Qiong La, Yonghong Zhou, Xiaoyun Pan. Phenotypic plasticity of Alternanthera philoxeroides in response to simulated daily warming: Introduced vs. native populations[J]. Biodiv Sci, 2021, 29(4): 419-427.

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URL: https://www.biodiversity-science.net/EN/10.17520/biods.2020387

https://www.biodiversity-science.net/EN/Y2021/V29/I4/419

Figures/Tables 2

Table 1 Effects of origin (i.e. introduced vs. native) and simulated daily warming (i.e. control vs. warming) and their interaction on fitness traits (total biomass, storage root biomass (STB)), functional traits (branching intensity (BI), specific stem length (SSL), root to shoot ratio (RSR) and specific leaf area (SLA)) and herbivorous effect (relative feeding area (RFA) and stem-tip feeding proportion (SFP)) of Alternanthera philoxeroides. Significant effects are marked in bold and marginally significant effects are marked in italics and bold.

变异来源Source of variation	总生物量 Total biomass		贮藏根生物量 STB		分枝强度 BI		比茎长 SSL		根冠比 RSR		比叶面积 SLA		相对取食面积 RFA		茎端取食率 SFP
变异来源Source of variation	χ²	P	χ²	P	χ²	P	χ²	P	χ²	P	χ²	P	χ²	P	χ²	P
增温 Warming (W)	5.165	0.023	3.207	0.073	4.239	0.040	0.761	0.383	0.343	0.558	0.021	0.884	0.083	0.773	10.552	0.001
来源地 Origin (O)	1.523	0.217	8.756	0.003	8.023	0.005	8.092	0.004	5.758	0.016	4.665	0.031	1.837	0.175	3.680	0.055
W × O	2.986	0.084	0.244	0.621	1.077	0.299	3.453	0.063	0.913	0.339	0.365	0.546	3.682	0.055	1.772	0.183

Fig. 1 Responses of introduced (China) and native (Argentina) populations of Alternanthera philoxeroides to simulated daily warming. Error bars indicate 95% confidence intervals, and ? indicate marginally significant differences in responses between introduced and native populations.

References 40

[1]	Beckmann M, Bruelheide H, Erfmeier A (2011) Germination responses of three grassland species differ between native and invasive origins. Ecological Research, 26,763-771.
[2]	Blumenthal DM, Kray JA, Ortmans W, Ziska LH, Pendall E (2016) Cheatgrass is favored by warming but not CO₂ enrichment in a semi-arid grassland. Global Change Biology, 22,3026-3038. DOI URL PMID
[3]	Buckland SM, Thompson K, Hodgson JG, Grime JP (2001) Grassland invasions: Effects of manipulations of climate and management. Journal of Applied Ecology, 38,301-309.
[4]	Burgin S, Norris A (2008) Alligator weed (Alternanthera philoxeroides) in New South Wales, Australia: A status report. Weed Biology and Management, 8,284-290.
[5]	Chu YM, Yang J, Li JJ, Peng PH (2014) Three warming scenarios differentially affect the morphological plasticity of an invasive herb Alternanthera philoxeroides. Acta Ecologica Sinica, 34,1411-1417. (in Chinese with English abstract)
	[ 褚延梅, 杨健, 李景吉, 彭培好 (2014) 三种增温情景对入侵植物空心莲子草形态可塑性的影响. 生态学报, 34,1411-1417. ]
[6]	Daehler CC (2003) Performance comparisons of co-occurring native and alien invasive plants: Implications for conservation and restoration. Annual Review of Ecology, Evolution, and Systematics, 34,183-211.
[7]	Dong BC, Alpert P, Zhang Q, Yu FH (2015) Clonal integration in homogeneous environments increases performance of Alternanthera philoxeroides. Oecologia, 179,393-403. URL PMID
[8]	Geng YP, Pan XY, Xu CY, Zhang WJ, Li B, Chen JK (2006) Phenotypic plasticity of invasive Alternanthera philoxeroides in relation to different water availability, compared to its native congener. Acta Oecologica, 30,380-385.
[9]	Griffith AB, Andonian K, Weiss CP, Loik ME (2014) Variation in phenotypic plasticity for native and invasive populations of Bromus tectorum. Biological Invasions, 16,2627-2638.
[10]	He WM, Li JJ, Peng PH (2012) Simulated warming differentially affects the growth and competitive ability of Centaurea maculosa populations from home and introduced ranges. PLoS ONE, 7,e31170. DOI URL PMID
[11]	Hyldgaard B, Brix H (2012) Intraspecies differences in phenotypic plasticity: Invasive versus non-invasive populations of Ceratophyllum demersum. Aquatic Botany, 97,49-56.
[12]	Julien MH, Skarratt B, Maywald GF (1995) Potential geographical-distribution of alligator weed and its biological-control Agasicles hygrophila. Journal of Aquatic Plant Management, 33,55-60.
[13]	Kim YU, Lee BW (2019) Differential mechanisms of potato yield loss induced by high day and night temperatures during tuber initiation and bulking: Photosynthesis and tuber growth. Frontiers in Plant Science, 10,300. URL PMID
[14]	Lemoine NP, Drews WA, Burkepile DE, Parker JD (2013) Increased temperature alters feeding behavior of a generalist herbivore. Oikos, 122,1669-1678.
[15]	Lin DL, Xia JY, Wan SQ (2010) Climate warming and biomass accumulation of terrestrial plants: A meta-analysis. New Phytologist, 188,187-198.
[16]	Liu M, Pan XY, Zhang ZJ, van Kleunen M, Li B (2020) Testing the shifting defense hypothesis for constitutive and induced resistance and tolerance. Journal of Pest Science, 93,355-364.
[17]	Liu M, Zhou F, Pan XY, Zhang ZJ, Traw MB, Li B (2018) Specificity of herbivore-induced responses in an invasive species, Alternanthera philoxeroides (Alligator weed). Ecology and Evolution, 8,59-70.
[18]	Luo YQ (2007) Terrestrial carbon-cycle feedback to climate warming. Annual Review of Ecology Evolution and Systematics, 38,683-712.
[19]	McKinney ML (2006) Urbanization as a major cause of biotic homogenization. Biological Conservation, 127,247-260.
[20]	Nguyen HM, Yadav NS, Barak S, Lima FP, Sapir Y, Winters G (2020) Responses of invasive and native populations of the seagrass Halophila stipulacea to simulated climate change. Frontiers in Marine Science, 6,812.
[21]	Nicotra AB, Atkin OK, Bonser SP, Davidson AM, Finnegan EJ, Mathesius U, Poot P, Purugganan MD, Richards CL, Valladares F, van Kleunen M (2010) Plant phenotypic plasticity in a changing climate. Trends in Plant Science, 15,684-692. DOI URL PMID
[22]	Pan XY, Geng YP, Sosa A, Zhang WJ, Li B, Chen JK (2007) Invasive Alternanthera philoxeroides: Biology, ecology and management. Acta Phytotaxonomica Sinica, 45,884-900. (in Chinese with English abstract)
	[ 潘晓云, 耿宇鹏, Alejandro Sosa, 张文驹, 李博, 陈家宽 (2007) 入侵植物喜旱莲子草——生物学、生态学及管理. 植物分类学报, 45,884-900. ]
[23]	Pan XY, Jia X, Fu DJ, Li B (2013) Geographical diversification of growth-defense strategies in an invasive plant. Journal of Systematics and Evolution, 51,308-317.
[24]	Paudel S, Lin PA, Hoover K, Felton GW, Rajotte EG (2020) Asymmetric responses to climate change: Temperature differentially alters herbivore salivary elicitor and host plant responses to herbivory. Journal of Chemical Ecology, 46,891-905.
[25]	Peng SS, Piao SL, Ciais P, Myneni RB, Chen AP, Chevallier F, Dolman AJ, Janssens IA, Peñuelas J, Zhang GX, Vicca S, Wan SQ, Wang SP, Zeng H (2013) Asymmetric effects of daytime and night-time warming on Northern Hemisphere vegetation. Nature, 501,88-92. URL PMID
[26]	Peng Y, Yang JX, Zhou XH, Peng PH, Li JJ, Zhang SM, He WM (2019) An invasive population of Solidago canadensis is less sensitive to warming and nitrogen-addition than its native population in an invaded range. Biological Invasions, 21,151-162.
[27]	Pereira FMV, Rosa E, Fahey JW, Stephenson KK, Carvalho R, Aires A (2002) Influence of temperature and ontogeny on the levels of glucosinolates in broccoli (Brassica oleracea var. italica) sprouts and their effect on the induction of mammalian phase 2 enzymes. Journal of Agricultural and Food Chemistry, 50,6239-6244.
[28]	Portela R, Dong BC, Yu FH, Barreiro R, Roiloa SR, Silva Matos DM (2020) Trans-generational effects in the clonal invader Alternanthera philoxeroides. Journal of Plant Ecology, 13,122-129.
[29]	Prange RK, McRae KB, Midmore DJ, Deng RB (1990) Reduction in potato growth at high temperature: Role of photosynthesis and dark respiration. American Potato Journal, 67,357-369.
[30]	R Development Core Team (2020) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna.
[31]	Richards CL, Bossdorf O, Muth NZ, Gurevitch J, Pigliucci M (2006) Jack of all trades, master of some? On the role of phenotypic plasticity in plant invasions. Ecology Letters, 9,981-993. URL PMID
[32]	Shipley B, Meziane D (2002) The balanced-growth hypothesis and the allometry of leaf and root biomass allocation. Functional Ecology, 16,326-331.
[33]	Wang Q, Tang Y, Xie T, Wang H (2017) Distinctive responses of photosynthetic characteristics to warming of invasive Alternanthera philoxeroides and native Sambucus chinensis. Acta Ecologica Sinica, 37,770-777. (in Chinese with English abstract)
	[ 王琼, 唐娅, 谢涛, 王辉 (2017) 入侵植物喜旱莲子草和本地种接骨草光合生理特征对增温响应的差异. 生态学报, 37,770-777. ]
[34]	Wu H, Zhang C, Dai WK (2020) Interactive effects of climate warming and species diversity on the invasiveness of the alien weed Alternanthera philoxeroides. Acta Prataculturae Sinica, 29,38-48. (in Chinese with English abstract)
	[ 吴昊, 张辰, 代文魁 (2020) 气候变暖和物种多样性交互效应对空心莲子草入侵的影响. 草业学报, 29,38-48. ]
[35]	Yu LR, Zhu ZC, Pan XY (2020) Phenotypic plasticity of Alternanthera philoxeroides in response to root neighbors of kin: Introduced vs. native genotypes. Biodiversity Science, 28,651-657. (in Chinese with English abstract)
	[ 于良瑞, 朱政财, 潘晓云 (2020) 喜旱莲子草对同基因型邻体根系的表型可塑性: 入侵地和原产地的比较. 生物多样性, 28,651-657. ]
[36]	Zhang R, Leshak A, Shea K (2012) Decreased structural defence of an invasive thistle under warming. Plant Biology, 14,249-252. URL PMID
[37]	Zhang ZJ, Zhou F, Pan XY, Kleunen M, Liu M, Li B (2019) Evolution of increased intraspecific competitive ability following introduction: The importance of relatedness among genotypes. Journal of Ecology, 107,387-395.
[38]	Zhang ZY, Zhang ZJ, Pan XY (2015) Phenotypic plasticity of Alternanthera philoxeroides in response to shading: Intro- duced vs. native populations. Biodiversity Science, 23,18-22. (in Chinese with English abstract)
	[ 张紫妍, 张致杰, 潘晓云 (2015) 喜旱莲子草对遮荫的可塑性反应: 入侵地与原产地种群的比较. 生物多样性, 23,18-22. ]
[39]	Zhou F, Zhang ZJ, Liu M, Pan XY (2017) Effects of nutrient levels on defense against specialist insects in an invasive alligator weed. Biodiversity Science, 25,1276-1284. (in Chinese with English abstract)
	[ 周方, 张致杰, 刘木, 潘晓云 (2017) 养分影响入侵种喜旱莲子草对专食性天敌的防御. 生物多样性, 25,1276-1284. ]
[40]	Zhou XH, He WM (2020) Climate warming facilitates seed germination in native but not invasive solidago canadensis populations. Frontiers in Ecology and Evolution, 8,595214.