Whole-plant Carbon and Nitrogen Allocation and Trade-off Strategies of Invasive Laguncularia racemosa and Native Avicennia marina across Dry and Wet Seasons

doi:10.7525/j.issn.1673-5102.2026.02.012

Abstract

Abstract:

Plant carbon（C） and nitrogen（N） stoichiometry reflects resource allocation strategies. However， current researches often focus on individual organs， overlooking the critical feedback between whole-plant and soil systems in natural habitats. This oversight is particularly critical in invaded mangrove ecosystems， where it limits the understanding of interspecific competition mechanisms. Here， this study investigated the invasive Laguncularia racemosa and the native Avicennia marina in Hainan， China. The C and N contents and C-to-N ratios were measured across leaves， branches， and roots， alongside key physicochemical properties of rhizosphere surface（0-10 cm） and subsurface（10-20 cm） soils in monoculture and mixed stands during both dry and wet seasons. Results showed that A. marina consistently maintained significantly higher N contents and lower C-to-N ratios across all organs compared to L. racemosa. Additionally， surface soil N contents were significantly higher in A. marina monocultures than in L. racemosa stands during the dry season， while soil C-to-N ratios remained lower. The dry season significantly strengthened root-branch stoichiometric linkages in L. racemosa， where all organs showed tight correlations with soil physicochemical factors at both soil depths. Conversely， A. marina exhibited whole-plant synergy only in the wet season； in the dry season， root-leaf and root-branch stoichiometric relationships were decoupled， and leaf and branch traits shifted to correlate closely with subsurface soil factors. During dry season， species mixing promoted widespread C and N associations across organs in A. marina and increased leaf C contents， while significantly elevating leaf N contents and reducing C-to-N ratios in L. racemosa during the wet season. This study revealed that the competitive advantage of L. racemosa was driven by its lower tissue construction costs and sustained coupling with soil resources during dry season. Notably， while mixed stand improved the inter-organ physiological coordination of the native A. marina， they allowed L. racemosa to more efficiently alleviate its nutrient limitations， thereby amplifying its invasive dominance. These findings highlighted a critical risk for mangrove restoration： interspecific facilitation may inadvertently accelerate the expansion of invasive species， potentially undermining management strategies.

Key words: Laguncularia racemosa, Avicennia marina, invasive plant, dry and wet seasons, carbon and nitrogen stoichiometry, plant-soil feedback, functional trait relationship

CLC Number:

S718.5

Hua YANG, Qihang LU, Yanjun DU, Wenna WANG. Whole-plant Carbon and Nitrogen Allocation and Trade-off Strategies of Invasive Laguncularia racemosa and Native Avicennia marina across Dry and Wet Seasons[J]. Bulletin of Botanical Research, 2026, 46(2): 336-347.

Figures/Tables 8

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References 53

[1]	CHEN X L， CHEN H Y H. Plant mixture balances terrestrial ecosystem C∶N∶P stoichiometry［J］.Nature Communications，2021，12：4562.
[2]	PEÑUELAS J， SARDANS J.The global nitrogen-phosphorus imbalance［J］.Science，2022，375（6578）：266-267.
[3]	LIU R， YANG X J， GAO R R，et al.Coordination of economics spectra in leaf，stem and root within the genus Artemisia along a large environmental gradient in China［J］.Global Ecology and Biogeography，2023，32（2）：324-338.
[4]	WRIGHT I J， REICH P B， WESTOBY M，et al.The worldwide leaf economics spectrum［J］.Nature，2004，428：821-827.
[5]	DÍAZ S， KATTGE J， CORNELISSEN J H C，et al.The global spectrum of plant form and function［J］.Nature，2016，529：167-171.
[6]	VAN KLEUNEN M， WEBER E， FISCHER M.A meta-analysis of trait differences between invasive and non-invasive plant species［J］.Ecology Letters，2010，13（2）：235-245.
[7]	HEBERLING J M， FRIDLEY J D.Resource-use strategies of native and invasive plants in Eastern North American forests［J］.New Phytologist，2013，200（2）：523-533.
[8]	RILOV G， CANNING-CLODE J， GUY-HAIM T.Ecological impacts of invasive ecosystem engineers：a global perspective across terrestrial and aquatic systems［J］.Functional Ecology，2024，38（1）：37-51.
[9]	FUNK J L， VITOUSEK P M.Resource-use efficiency and plant invasion in low-resource systems［J］.Nature，2007，446（7139）：1079-1081.
[10]	STOTZ G C， SALGADO-LUARTE C， ESCOBEDO V M，et al.Phenotypic integration limits the variation in plant phenotypic plasticity among traits：a meta-analysis［J］.Functional Ecology，2025，39（11）：3021-3033.
[11]	HE N P， LI Y， LIU C C，et al.Plant trait networks：improved resolution of the dimensionality of adaptation［J］.Trends in Ecology & Evolution，2020，35（10）：908-918.
[12]	MATESANZ S， BLANCO-SÁNCHEZ M， RAMOS-MUÑOZ M，et al.Phenotypic integration does not constrain phenotypic plasticity：differential plasticity of traits is associated to their integration across environments［J］.New Phytologist，2021，231（6）：2359-2370.
[13]	CARRILLO Y， BELL C， KOYAMA A，et al.Plant traits，stoichiometry and microbes as drivers of decomposition in the rhizosphere in a temperate grassland［J］.Journal of Ecology，2017，105（6）：1750-1765.
[14]	TESTE F P， KARDOL P， TURNER B L，et al.Plant-soil feedback and the maintenance of diversity in Mediterranean-climate shrublands［J］.Science，2017，355（6321）：173-176.
[15]	CHENG J K， YU S X.Nitrogen allocation among leaves and roots mediates the interaction between plant life history trade-off and density dependence［J］.Frontiers in Plant Science，2025，16：1549801.
[16]	GOLDBERG L， LAGOMASINO D， THOMAS N，et al.Global declines in human-driven mangrove loss［J］.Global Change Biology，2020，26（10）：5844-5855.
[17]	BAI J K， MENG Y C， GOU R K，et al.The linkages between stomatal physiological traits and rapid expansion of exotic mangrove species （Laguncularia racemosa） in new territories［J］.Frontiers in Marine Science，2023，10：1136443.
[18]	LI H K， CHEN C L， ZHOU J Y，et al.Exotic mangrove Laguncularia racemosa litter input accelerates nutrient cycling in mangrove ecosystems［J］.Frontiers in Plant Science，2024，15：1463548.
[19]	SOBUJ N， SINGH K， BYUN C.Responses of invasive and native plant species to drought stress and elevated CO₂ concentrations：a meta-analysis［J］.NeoBiota，2024，96：381-401.
[20]	COHEN I， ZANDALINAS S I， HUCK C，et al.Meta-analysis of drought and heat stress combination impact on crop yield and yield components［J］.Plant Physiology，2021，171（1）：66-76.
[21]	CARDONA-OLARTE P， KRAUSS K W， TWILLEY R R.Leaf gas exchange and nutrient use efficiency help explain the distribution of two neotropical mangroves under contrasting flooding and salinity［J］.International Journal of Forestry Research，2013，2013（1）：524625.
[22]	NGUYEN H T， STANTON D E， SCHMITZ N，et al.Growth responses of the mangrove Avicennia marina to salinity：development and function of shoot hydraulic systems require saline conditions［J］.Annals of Botany，2015，115（3）：397-407.
[23]	LEISHMAN M R， HASLEHURST T， ARES A，et al.Leaf trait relationships of native and invasive plants：community- and global-scale comparisons［J］.New Phytologist，2007，176（3）：635-643.
[24]	WANG L M， MU M R， LI X F，et al.Differentiation between true mangroves and mangrove associates based on leaf traits and salt contents［J］.Journal of Plant Ecology，2011，4（4）：292-301.
[25]	陈毅青，陈宗铸，陈小花，等.石梅湾3种植物叶片与其群落凋落物C，N，P生态化学计量特征研究［J］.林业资源管理，2020，（4）：66-73.
	CHEN Y Q， CHEN Z Z， CHEN X H，et al.A study on ecological stoichiometric characteristics of C，N and P in three kinds of plant leaves and their community litters in Shimeiwan of Hainan Island［J］.Forest and Grassland Resources Research，2020，（4）：66-73.
[26]	ADLER P B， SALGUERO-GÓMEZ R， COMPAGNONI A，et al.Functional traits explain variation in plant life history strategies［J］.Proceedings of the National Academy of Sciences of the United States of America，2014，111（2）：740-745.
[27]	FRESCHET G T， ROUMET C， COMAS L H，et al.Root traits as drivers of plant and ecosystem functioning：current understanding，pitfalls and future research needs［J］.New Phytologist，2021，232（3）：1123-1158.
[28]	PÉREZ A， MACHADO W， SANDERS C J.Anthropogenic and environmental influences on nutrient accumulation in mangrove sediments［J］.Marine Pollution Bulletin，2021，165：112174.
[29]	WANG Y， LI D Y， LU Z Q，et al.Decomposition and variation in carbon and nitrogen of leaf litter mixtures in a subtropical mangrove forest［J］.Forests，2024，15（4）：672.
[30]	CHAO L， LIU Y Y， FRESCHET G T，et al.Litter carbon and nutrient chemistry control the magnitude of soil priming effect［J］.Functional Ecology，2019，33（5）：876-888.
[31]	HANDA I T， AERTS R， BERENDSE F，et al.Consequences of biodiversity loss for litter decomposition across biomes［J］.Nature，2014，509：218-221.
[32]	JOLY F X， FROMIN N， KIIKKILÄ O，et al.Diversity of leaf litter leachates from temperate forest trees and its consequences for soil microbial activity［J］.Biogeochemistry，2016，129：373-388.
[33]	SANTONJA M， RANCON A， FROMIN N，et al.Plant litter diversity increases microbial abundance，fungal diversity，and carbon and nitrogen cycling in a Mediterranean shrubland［J］.Soil Biology and Biochemistry，2017，111：124-134.
[34]	REEF R， FELLER I C， LOVELOCK C E.Nutrition of mangroves［J］.Tree Physiology，2010，30（9）：1148-1160.
[35]	YU Z W， WANG M L， SUN Z Y，et al.Changes in the leaf functional traits of mangrove plant assemblages along an intertidal gradient in typical mangrove wetlands in Hainan，China［J］.Global Ecology and Conservation，2023，48：e02749.
[36]	LIU Q Y， WANG H M， XU X L.Root nitrogen acquisition strategy of trees and understory species in a subtropical pine plantation in southern China［J］.European Journal of Forest Research，2020，139（5）：791-804.
[37]	HU G， ZHANG Z H， LI L.Responses of carbon，nitrogen，and phosphorus contents and stoichiometry in soil and fine roots to natural vegetation restoration in a tropical mountainous area，southern China［J］.Frontiers in Plant Science，2023，14：1181365.
[38]	WANG J X， VILLAR-SALVADOR P， LI G L，et al.Moderate water stress does not inhibit nitrogen remobilization，allowing fast growth in high nitrogen content Quercus variabilis seedlings under dry conditions［J］.Tree Physiology，2019，39（4）：650-660.
[39]	HEINEMANN B， HILDEBRANDT T M.The role of amino acid metabolism in signaling and metabolic adaptation to stress-induced energy deficiency in plants［J］.Journal of Experimental Botany，2021，72（13）：4634-4645.
[40]	ZAYED O， HEWEDY O A， ABDELMOTELEB A，et al.Nitrogen journey in plants：from uptake to metabolism，stress response，and microbe interaction［J］.Biomolecules，2023，13（10）：1443.
[41]	LIANG S Y， TAN T， WU D Z，et al.Seasonal variations in carbon，nitrogen，and phosphorus of Pinus yunnanensis at different stand ages［J］.Frontiers in Plant Science，2023，14：1107961.
[42]	HASHIMOTO Y， MASUMOTO T， ITO T，et al.Can fine-root non-structural carbohydrates explain seasonal variations in the respiration in subalpine forests？［J］.Physiologia Plantarum，2025，177（6）：e70615.
[43]	ROBERT E M， SCHMITZ N， COPINI P，et al.Visualization of the stem water content of two genera with secondary phloem produced by successive cambia through Magnetic Resonance Imaging （MRI）［J］.Journal of Plant Hydraulics，2014，1：e0006.
[44]	LOVELOCK C E， BALL M C， FELLER I C，et al.Variation in hydraulic conductivity of mangroves：influence of species，salinity，and nitrogen and phosphorus availability［J］.Physiologia Plantarum，2006，127（3）：457-464.
[45]	REEF R， MARKHAM H L， SANTINI N S，et al.The response of the mangrove Avicennia marina to heterogeneous salinity measured using a split-root approach［J］.Plant and Soil，2015，393（1）：297-305.
[46]	WEI L L， LOCKINGTON D A， POH S C，et al.Water use patterns of estuarine vegetation in a tidal creek system［J］.Oecologia，2013，172（2）：485-494.
[47]	ZIPFEL C， OLDROYD G E D.Plant signalling in symbiosis and immunity［J］.Nature，2017，543：328-336.
[48]	SURIYAGODA L D B， RYAN M H， GILLE C E，et al.Phosphorus fractions in leaves［J］.New Phytologist，2023，237（4）：1122-1135.
[49]	MÉNDEZ-ALONZO R， LÓPEZ-PORTILLO J， MOCTEZUMA C，et al.Osmotic and hydraulic adjustment of mangrove saplings to extreme salinity［J］.Tree Physiology，2016，36（12）：1562-1572.
[50]	SOBRADO M A.Relationship of water transport to anatomical features in the mangrove Laguncularia racemosa grown under contrasting salinities［J］.New Phytologist，2007，173（3）：584-591.
[51]	SUÁREZ N.Leaf longevity，construction，and maintenance costs of three mangrove species under field conditions［J］.Photosynthetica，2003，41（3）：373-381.
[52]	KOMIYAMA A， ONG J E， POUNGPARN S.Allometry，biomass，and productivity of mangrove forests：a review［J］.Aquatic Botany，2008，89（2）：128-137.
[53]	LANG'AT J K S， KIRUI B K Y， SKOV M W，et al.Species mixing boosts root yield in mangrove trees［J］.Oecologia，2013，172（1）：271-278.

土层 Soil layer/cm	季节 Season	群落类型 Stand type	全氮 Total nitrogen/ （g·kg^-1）	全碳 Total carbon/ （g·kg^-1）	碳氮比 Carbon-to- nitrogen ratio	电导率 Electric conductivity/ （mS·cm^-1）	酸碱度 pH	含水量 Water content/%
［0，10）	雨季 Wet season	Lr-P	0.05±0.01^A*	4.27±0.63^A	93.43±8.21^A*	3.24±1.30^A	7.53±0.07^A	12.57±1.62^A
		Am-P	0.06±0.02^A*	3.25±0.53^A	55.55±0.37^B*	2.22±0.09^A	7.30±0.06^AB	12.50±2.58^A
		Lr-Am-M	0.08±0.02^A*	4.95±1.18^A	62.88±4.95^B*	2.42±0.16^A	7.20±0.12^B	13.62±2.37^A
	旱季 Dry season	Lr-P	0.32±0.04^B*	5.77±0.50^A	17.05±2.61^A*	5.75±4.09^A	7.37±0.15^A	15.25±5.09^A
		Am-P	0.62±0.07^A*	6.25±1.31^A	10.02±1.72^B*	5.07±2.01^A	7.27±0.27^A	17.52±2.88^A
		Lr-Am-M	0.39±0.02^B*	3.32±0.17^B	8.95±0.80^B*	3.48±1.07^A	7.13±0.07^A	15.98±1.30^A
［10，20］	雨季 Wet season	Lr-P	0.04±0.00^A*	2.76±0.54^A	79.14±10.57^A*	8.23±2.17^A	7.37±0.09^A	14.23±1.99^A
		Am-P	0.05±0.02^A*	3.21±1.64^A	49.41±7.10^B*	5.10±2.54^A	7.30±0.12^A	12.81±2.17^A
		Lr-Am-M	0.06±0.01^A*	3.71±0.82^A	56.70±2.78^B*	5.08±1.22^A	7.33±0.07^A	17.44±2.46^A
	旱季 Dry season	Lr-P	0.25±0.11^A*	3.80±0.99^A	17.55±1.64^A*	6.10±3.15^A	7.33±0.26^A	15.28±5.07^A
		Am-P	0.31±0.07^A*	2.81±0.69^A	9.47±1.34^B*	2.79±0.85^A	7.27±0.07^A	9.91±2.08^A
		Lr-Am-M	0.34±0.01^A*	2.84±0.17^A	8.50±0.29^B*	3.00±0.62^A	7.23±0.09^A	15.45±0.33^A

变量 Variable	全碳 Total carbon/（g·kg^-1）			全氮 Total nitrogen/（g·kg^-1）			碳氮比 Carbon-to-nitrogen ratio
变量 Variable	自由度 d_f	F	P	自由度d_f	F	P	自由度d_f	F	P
季节 Seasons	1	19.53	<0.01	1	3.84	0.06	1	0.10	0.75
树种 Tree species	1	2.14	0.15	1	228.83	<0.01	1	54.16	<0.01
器官 Organs	2	136.83	<0.01	2	130.68	<0.01	2	17.36	<0.01
季节×树种 Seasons×Tree species	1	0.12	0.73	1	2.35	0.13	1	0.02	0.88
季节×器官 Seasons×Organs	2	1.88	0.16	2	1.39	0.26	2	4.16	0.02
树种×器官 Tree species×Organs	2	1.01	0.37	2	19.14	<0.01	2	5.73	<0.01
季节×树种×器官 Seasons×Tree species×Organs	2	1.37	0.26	2	1.36	0.27	2	3.84	0.03

土壤深度 Soil depth/cm	季节 Season	树种 Tree species	关联类型 Relationship type
土壤深度 Soil depth/cm	季节 Season	树种 Tree species	叶 Leaf	土壤 Soil	相关系数 r	枝 Branch	土壤 Soil	相关系数 r	根 Root	土壤 Soil	相关系数 r
［0，10）	雨季 Wet season	拉关木Lr	N	pH	-0.883*	C	N	0.971**	C∶N	含水量	0.829*
			C∶N	pH	0.883*	C	C	1.000**
						C	含水量	0.943**
		白骨壤Am			ns	C	N	0.928**	C	电导率	0.829*
						C	含水量	0.886*	N	电导率	-0.943**
									C∶N	电导率	0.829*
									C∶N	pH	-0.883*
	旱季 Dry season	拉关木Lr	C	电导率	0.841*	C	N	-0.886*	N	C	-0.829*
			C	含水量	0.829*				N	C∶N	-0.829*
			C∶N	C	0.829*				C∶N	C	0.829*
			C∶N	C∶N	0.829*				C∶N	C∶N	0.829*
		白骨壤Am			ns			ns			ns
［10，20］	雨季 Wet season	拉关木Lr			ns			ns	C∶N	C	0.829*
		拉关木Lr			ns			ns	C∶N	含水量	0.943**
		白骨壤Am			ns	C	N	0.943*	C	电导率	-0.829*
		白骨壤Am			ns	C	C	0.829*
	旱季 Dry season	拉关木Lr	C	C	0.829*	C	C∶N	0.829*	N	C∶N	-0.829*
		拉关木Lr	C∶N	C∶N	0.829*				C∶N	C∶N	0.829*
		白骨壤Am	C∶N	含水量	0.886*	C	N	0.829*			ns
		白骨壤Am				C∶N	电导率	-0.886*			ns